Abstract
Apoptosis is characterized by the programmed activation of specific biochemical pathways leading to the organized demise of cells. To date, aspects of the intracellular signaling machinery involved in this phenomenon have been extensively dissected and characterized. However, recent studies have elucidated a novel role for changes in the intracellular milieu of the cells as important modulators of the cell death program. Specially, intracellular ionic homeostasis has been reported to be a determinant in both the activation and progression of the apoptotic cascade. Several apoptotic insults trigger specific changes in ionic gradients across the plasma membrane leading to depolarization of the plasma membrane potential (PMP). These changes lead to ionic imbalance early during apoptosis. Several studies have also suggested the activation and/or modulation of specific ionic transport mechanisms including ion channels, transporters and ATPases, as mediators of altered intracellular ionic homeostasis leading to PMP depolarization during apoptosis. However, the role of PMP depolarization and of the changes in ionic homeostasis during the progression of apoptosis are still unclear. This review summarizes the current knowledge regarding the causes and consequences of PMP depolarization during apoptosis. We also review the potential electrogenic ion transport mechanisms associated with this event, including the net influx/efflux of cations and anions. An understanding of these mechamisms could lead to the generation of new therapeutic approaches for a variety of diseases involving apoptosis.
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Abbreviations
- AVD,:
-
apoptotic volume decrease;
- PMP,:
-
plasma membrane potential;
- RVD,:
-
regulatory volume decrease;
- VGNC,:
-
voltage-gated Na+ channel;
- VGCC, :
-
voltage-gated Ca2+ channels.
References
Aarts M., lihara K., Wei W.L., Xiong Z.G., Arundine M., Cerwinski W., MacDonald J.F., Tymianski M. 2003. A key role for TRPM7 channels in anoxic neuronal death. Cell. 115:863–877
Aarts, M.M., Tymianski, M. 2005. TRPMs and neuronal cell death. Pfluegers Arch. 451:243–249
Agopyan N., Bhatti T., Yu S., Simon S.A. 2003. Vanilloid receptor activation by 2- and 10-microm particles induces responses leading to apoptosis in human airway epithelial cells. Toxicol. Appl. Pharmacol. 192:21–35
Agopyan N., Head J., Yu S., Simon S.A. 2004. TRPV1 receptors mediate particulate matter-induced apoptosis. Am. Physiol. 286:L563–L572
Annunziato L., Pignataro G., Di Renzo G.F. 2004. Pharmacology of brain Na+/Ca2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol. Rev. 56:633–654
Apell H.J. 2003. Structure-function relationship in P-type ATPases—a biophysical approach. Rev. Physiol. Biochem. Pharmacol. 150:1–35
Arcangeli A., Becchetti A., Mannini A., Mugnai G., De Filippi P., Tarone G., Del Bene M.R., Barletta E., Wanke E., Olivotto M. 1993. Integrin-mediated neurite outgrowth in neuroblastoma cells depends on the activation of potassium channels. J. Cell Biol. 122:1131–1143
Ares M.P., Porn-Ares M.I., Thyberg J., Juntti-Berggren L., Berggren P.O., Diczfalusy U., Kallin B., Bjorkhem I., Orrenius S., Nilsson J. 1997. Ca2+ channel blockers verapamil and nifedipine inhibit apoptosis induced by 25-hydroxycholesterol in human aortic smooth muscle cells. J. Lipid Res. 38:2049–2061
Arrebola F., Zabiti S., Canizares F.J., Cubero M.A., Crespo P.V., Fernandez-Segura E. 2005. Changes in intracellular sodium, chlorine, and potassium concentrations in staurosporine-induced apoptosis. J. Cell Physiol. 204:500–507
Ba F., Pang P.K., Benishin C.G. 2004. The role of Ca2+ channel modulation in the neuroprotective actions of estrogen in beta-amyloid protein and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) cytotoxic models. Neurochem. Int. 45:31–38
Banasiak K.J., Burenkova O., Haddad G.G. 2004. Activation of voltage-sensitive sodium channels during oxygen deprivation leads to apoptotic neuronal death. Neuroscience. 126:31–44
Barone F., Aguanno S., D′Agostino A. 2005. Modulation of MAA-induced apoptosis in male germ cells: role of Sertoli cell P/Q-type calcium channels. Reprod. Biol. Endocrinol. 3:13
Barone F., Aguanno S., D′Alessio A., D′Agostino A. 2004. Sertoli cell modulates MAA-induced apoptosis of germ cells throughout voltage-operated calcium channels. FASEB J. 18:353–354
Berridge M.J., Bootman M.D., Roderick H.L. 2003. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rey. Mol. Cell Biol. 4:517–529
Bodo E., Biro T., Telek A., Czifra G., Griger Z., Toth B.I., Mescalchin A., Ito T., Bettermann A., Kovacs L, Paus R. 2005. A hot new twist to hair biology: involvement of vanilloid receptor-1 (VR1/TRPV1) signaling in human hair growth control. Am. J. Pathol. 166:985–998
Bortner C.D., Cidlowski J.A. 2002. Apoptotic volume decrease and the incredible shrinking cell. Cell Death Differ. 9:1307–1310
Bortner C.D., Cidlowski J.A. 2003. Uncoupling cell shrinkage from apoptosis reveals that Na+ influx is required for volume loss during programmed cell death. J. Biol. Chem. 278:39176–39184
Bortner C.D., Cidlowski J.A. 2004. The role of apoptotic volume decrease and ionic homeostasis in the activation and repression of apoptosis. Pfluegers Arch. 448:313–318
Bortner C.D., Gomez-Angelats M., Cidlowski J.A. 2001. Plasma membrane depolarization without repolarization is an early molecular event in anti-Fas-induced apoptosis. J. Biol. Chem. 276:4304–4314
Bortner C.D., Hughes F.M., Jr., Cidlowski J.A. 1997. A primary role for K+ and Na+ efflux in the activation of apoptosis. J. Bio. Chem. 272:32436–32442
Borzi R.M., Mazzetti I., Magagnoli G., Paoletti S., Uguccioni M., Gatti R., Orlandini G., Cattini L., Facchini A. 2002. Growth-related oncogene alpha induction of apoptosis in osteoarthritis chondrocytes. Arthritis Rheum. 46:3201–3211
Brassard D.L., Maxwell E., Malkowski M., Nagabhushan T.L., Kumar C.C., Armstrong L. 1999. Integrin alpha(v)beta(3)-mediated activation of apoptosis. Exp. Cell Res. 251:33–45
Callaway J.K., Beart P.M., Jarrott B., Giardina S.F. 2001. Incorporation of sodium channel blocking and free radical scavenging activities into a single drug, AM-36, results in profound inhibition of neuronal apoptosis. Br. J. Pharmacol. 132:1691–1698
Cano-Abad M.F., Villarroya M., Garcia A.G., Gabilan N.H., Lopez M.G. 2001. Calcium entry through L-type calcium channels causes mitochondria disruption and chromaffin cell death. J. Biol. Chem. 276:39695–39704
Carter A.J. 19980. The importance of voltage-dependent sodium channels in cerebral ischaemia. Amino Acids 14:159–169
Chacon-Cruz E., Oelberg D.G., Davis P., Buescher E.S. 1998. Membrane depolarization and depletion of intracellular calcium stores are associated with delay of apoptosis in human neutrophils. J. Leukoc. Biol. 64:759–766
Chakraborti T., Ghosh S.K., Michael J.R., Batabyal S.K., Chakraborti S. 1998. Targets of oxidative stress in cardiovascular system. Mol. Cell Biochem. 187:1–10
Chami M., Ferrari D., Nicotera P., Paterlini-Brechot P., Rizzuto R. 2003. Caspase-dependent alterations of Ca2+ signaling in the induction of apoptosis by hepatitis B virus X protein. J. Biol. Chem. 278:31745–31755
Chatterjee M.L., Roy A.R. 1965. Toxic effects of ouabain on the isolated heart of reserpinised rabbit. Bull. Calcutta Sch. Trop. Med. 13:54–57
Chauhan N.B., Lee J.M., Siegel G.J. 1997. Na,K-ATPase mRNA levels and plaque load in Alzheimer’s disease. J. Mol. Neurosci. 9:151–166
Chifflet S., Correa V., Nin V., Justet C., Hernandez J.A. 2004. Effect of membrane potential depolarization on the organization of the actin cytoskeleton of eye epithelia. The role of adherens junctions. Exp. Eye Res. 79:769–777
Chifflet S., Hernandez J.A., Grasso S., Cirillo A. 2003. Nonspecific depolarization of the plasma membrane potential induces cytoskeletal modifications of bovine corneal endothelial cells in culture. Exp. Cell Res. 282:1–13
Chueh S.C., Guh J.H., Chen J., Lai M.K., Teng C.M. 2001. Dual effects of ouabain on the regulation of proliferation and apoptosis in human prostatic smooth muscle cells. dJJrol. 166:347–353
Cimen B., Turkozkan N., Seven I., Unlu A., Karasu C. 2004. Impaired Na+,K+- ATPase activity as a mechanism of reactive nitrogen species-induced cytotoxicity in guinea pig liver exposed to lipopolysaccharides. Mol. Cell. Biochem. 259:53–57
Courageot M.P., Lepine S., Hours M., Giraud F., Sulpice J.C. 2004. Involvement of sodium in early phosphatidylserine exposure and phospholipid scrambling induced by P2X7 purinoceptor activation in thymocytes. J. Biol. Chem. 279:21815–21823
Croft D.R., Coleman M.L., Li S., Robertson D., Sullivan T., Stewart C.L., Olson M.F. 2005. Actin-myosin-based contraction is responsible for apoptotic nuclear disintegration. J. Cell Biol. 168:245–255
Dallaporta B., Marchetti P., de Pablo MA, Maisse C., Due H.T., Metivier D., Zamzami N., Geuskens M., Kroemer G. 1999. Plasma membrane potential in thymocyte apoptosis. J. Immunol. 162:6534–6542
d’Anglemont de Tassigny A., Souktani R., Henry P., Ghaleh B., Berdeaux A. 2004. Volume-sensitive chloride channels (ICI,vol) mediate doxorubicin-induced apoptosis through apoptotic volume decrease in cardiomyocytes. Fundam. Clin. Pharmacol. 18:531–538
Dargent B., Arsac C., Tricaud N., Couraud F. 1996. Activation of voltage-dependent sodium channels in cultured cerebellar poffule cells induces neurotoxicity that is not mediated by glutamate release. Neuroscience 73:209–216
Detre, C., Kiss, E., Varga, Z., Ludanyi, K., Paszty, K., Enyedi, A., Kovesdi, D., Panyi, G., Rajnavolgyi, E., Matko, J. 2006. Death or survival: Membrane ceramide controls the fate and activation of antigen-specific T-cells depending on signal strength and duration. Cell Signal 18:294–306
Diss J.K., Fraser S.P., Djamgoz M.B. 2004. Voltage-gated Na+ channels: multiplicity of expression, plasticity, functional implications and pathophysiological aspects. Eur. Biophys. J. 33:180–193
Dupere-Minier G., Hamelin C., Desharnais P., Bernier J. 2004. Apoptotic volume decrease, pH acidification and chloride channel activation during apoptosis requires CD45 expression in HPB-ALL T cells. Apoptosis 9:543–551
Dussmann H., Kogel D., Rehm M., Prehn J.H. 2003a. Mitochondrial membrane permeabilization and superoxide production during apoptosis. A single-cell analysis. J. Biol. Chem. 278:12645–12649
Dussmann H., Rehm M., Kogel D., Prehn J.H. 2003b. Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J. Cell Sci. 116:525–536
Eguchi Y., Srinivasan A., Tomaselli K.J., Shimizu S., Tsujimoto Y. 1999. ATP-dependent steps in apoptotic signal transduction. Cancer Res. 59:2174–2181
Eigel B.N., Gursahani H., Hadley R.W. 2004. Na+/Ca2+ exchanger plays a key role in inducing apoptosis after hypoxia in cultured guinea pig ventricular myocytes. Am. J. Physiol 287:H1466–1475
Elinder F., Akanda N., Tofighi R., Shimizu S., Tsujimoto Y., Orrenius S., Ceccatelli S. 2005. Opening of plasma membrane voltage-dependent anion channels (VDAC) precedes caspase activation in neuronal apoptosis induced by toxic stimuli. Cell Death Differ. 12:1134–1140
Estacion M., Schilling W.P. 2002. Blockade of maitotoxin-induced oncotic cell death reveals zeiosis. BMC PhysioL 2:2
Esteves M.B., Marques-Santos L.F., Affonso-Mitidieri O.R., Rumjanek V.M. 2005. Ouabain exacerbates activation-induced cell death in human peripheral blood lymphocytes. An. Acad. BraS. Cienc. 77:281–292
Friis M.B., Friborg C.R., Schneider L., Nielsen M.B., Lambert I.H., Christensen ST., Hoffmann E.K. 2005. Cell shrinkage as a signal to apoptosis in NIH 3T3 fibroblasts. J. Physiol. 567:427–443
Fujita H., Yanagisawa A., Ishikawa K. 1997. Suppressive effect of a chloride bicarbonate exchanger inhibitor on staurosporine-induced apoptosis of endothelial cells. Heart Vessels. Suppl 12:84–88
Garcia M.L, Usachev Y.M., Thayer S.A., Strehler E.E., Windebank A.J. 2001. Plasma membrane calcium ATPase plays a role in reducing Ca2+ mediated cytotoxicity in PC12 cells. J. Neurosci Res. 64:661–669
Gilbert M., Knox S. 1997. Influence of Bcl-2 overexpression on Na+/K+- ATPase pump activity: correlation with radiation-induced programmed cell death. JCellPhysiol. 171:299–304
Gilbert M.S., Saad A.M., Rupnow B.A., Knox S.J. 1996. Association of BCL-2 with membrane hyperpolarization and radioresistance. J. Cell Physiol. 168:114–122
Gil-Parrado S., Fernandez-Montalvan A., Assfalg-Machleidt I., Popp O., Bestvater F., Holloschi A., Knoch T.A., Auerswald E.A., Welsh K., Reed J.C., Fritz H., Fuentes-Prior P., Spiess E., Salvesen G.S., Machleidt W. 2002. lonomycin-activated calpain triggers apoptosis. A probable role for Bcl-2 family members. J. Biol. Chem. 277:27217–27226
Goldin A.L. 2001. Resurgence of sodium channel research. AnnuRe&Physiol. 63:871–894
Gomez-Lazaro, M., Galindo, M.F., Fernandez-Gomez, F.J., Prehn, J.H., Jordan, J. 2005. Activation of p53 and the pro-apoptotic p53 target gene PUMA during depolarization-induced apoptosis of chromaffin cells. Exp. Neurol. 196:96–103
Gonzalez Deniselle M.C., Lopez Costa J.J., Gonzalez S.L., Labombarda F., Garay L., Guennoun R., Schumacher M., De Nicola A.F. 2002. Basis of progesterone protection in spinal cord neurodegeneration. J. Steroid Biochem. Mol. Biol. 83:199–209
Grammatopoulos T.N., Johnson V., Moore S.A., Andres R., Weyhenmeyer J.A. 2004. Angiotensin type 2 receptor neuroprotection against chemical hypoxia is dependent on the delayed rectifier K+ channel, Na+ Ca2+ exchanger and Na+K+ ATPase in primary cortical cultures. Neurosci. Res. 50:299–306
Grassi C., D′Ascenzo M., Torsello A., Martinotti G., Wolf F., Cittadini A., Azzena G.B. 2004. Effects of 50 Hz electromagnetic fields on voltage-gated Ca2+ channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium. 35:307–315
Green D.R. 2003. Overview: apoptotic signaling pathways in the immune system. Immunol Rev. 193:5–9
Gulbins E., Welsch J., Lepple-Wienhuis A., Heinle H., Lang F. 1997. Inhibition of Fas-induced apoptotic cell death by osmotic cell shrinkage. Biochem. Biophys. Res. Commun. 236:517–521
Gutierrez A.A., Arias J.M., Garcia L, Mas-Oliva J., Guerrero-Hernandez A. 1999, Activation of a Ca2+-permeable cation channel by two different inducers of apoptosis in a human prostatic cancer cell line. J. Physiol. 517:95–107
Gwag B.J., Canzoniero L.M., Sensi S.L., Demaro J.A., Koh J.Y., Goldberg M.P., Jacquin M., Choi D.W. 1999. Calcium ionophores can induce either apoptosis or necrosis in cultured cortical neurons. Neurosciencel 90:1339–1348
Hajnoczky G., Davies E., Madesh M. 2003. Calcium signaling and apoptosis. Biochem. Biophy. Rev. Commun. 304:445–454
Hara Y., Wakamori M., Ishii M., Maeno E., Nishida M., Yoshida T., Yamada H., Shimizu S., Mori E., Kudoh J., Shimizu N., Kurose H., Okada Y., Imoto K., Mori Y. 2002. LTRPC2 Ca+permeable channel activated by changes in redox status confers susceptibility to cell death. Mol. Cell. 9:163–173
Hennion J.P., el-Masri MA, Huff M.O., el-Mailakh R.S. 2002. Evaluation of neuroprotection by lithium and valproic acid against ouabain-induced cell damage. Bipolar Disord. 4:201–206
Ho R., Ortiz D., Shea T.B. 2001. Amyloid-beta promotes calcium influx and neurodegeneration via stimulation of L voltage-sensitive calcium channels rather than NMDA channels in cultured neurons. J. Alzheimers Dis. 3:479–483
Hong Y.S., Park S., Geng C., Baek K., Bowman J.D., Yoon J., Pak W.L. 2002. Single amino acid change in the fifth transmembrane segment of the TRP channel causes massive degeneration of photoreceptors. J. Biol. Chem. 277:33884–33889
Howes A.L., Arthur J.F., Zhang T., Miyamoto S., Adams J.W., Dorn I.G., Woodcock E.A., Brown J.H. 2003. Akt-mediated cardiomyocyte survival pathways are compromised by G alpha q-induced phosphoinositide 4,5-bisphosphate depletion. J BioLChem. 278:40343–40351
Huang Y.T., Chueh S.C., Teng C.M., Guh J.H. 2004. Investigation of ouabain-induced anticancer effect in human androgen-independent prostate cancer PC-3 cells. Biochem. Pharmacol. 67:727–733
Jakab M., Furst J., Gschwentner M., Botta G., Garavaglia M.L., Bazzini C., Rodighiero S., Meyer G., Eichmueller S., Woll E., Chwatal S., Ritter M., Paulmichl M. 2002. Mechanisms sensing and modulating signals arising from cell swelling. Cell Physiol Biochem. 12:235–258
Jentsch T.J., Hubner C.A., Fuhrmann J.C. 2004. Ion channels: function unravelled by dysfunction. Nat Cell BioL 6:1039–1047
Jentsch T.J., Poet M., Fuhrmann J.C., Zdebik A.A. 2005. Physiological functions of CLC Cl- channels gleaned from human genetic disease and mouse models. Annu. Rev. Physiol. 67:779–807
Jeulin C., Dazy A.C., Marano F. 2002. Effects of hydrogen peroxide and hydroxyl radicals on the cytosolic side of a non-selective cation channel in the cultured human bronchial epithelial cell line 16HBE14o. Pfluegers Arch. 443:574–583
Johnson K., D’Mello S.R. 2005. p21-Activated kinase-1 is necessary for depolarization-mediated neuronal survival. J. Neurosci. Res. 79:809–815
Jordan J., Galindo M.F., Calvo S., Gonzalez-Garcia C., Cena V. 2000. Veratridine induces apoptotic death in bovine chromaffin cells through superoxide production. Br. J. PharmacoL 137:1496–1504
Jordan J., Galindo M.F., Gonzalez-Garcia C., Cena V. 2003. Role and regulation of p53 in depolarization-induced neuronal death. Neuroscience 122:707–715
Jordan J., Galindo M.F., Tornero D., Benavides A., Gonzalez C., Agapito M.T., Gonzalez-Garcia C., Cena V. 2002. Superoxide anions mediate veratridine-induced cytochrome c release and caspase activity in bovine chromaffin cells. J. Pharmacol. 137:993–1000
Jornot L., Petersen H., Junod A.F. 1998. Hydrogen peroxide-induced DMA damage is independent of nuclear calcium but dependent on redox-active ions. Biochem. J. 335:85–94
Kawazoe N., Aiuchi T., Masuda Y., Nakajo S., Nakaya K. 1999. Induction of apoptosis by bufalin in human tumor cells is associated with a change of intracellular concentration of Na+ ions. J. Biochem. (Tokyo) 126:278–286
Kim A.H., Sheline C.T., Tian M., Higashi T., McMahon R.J., Cousins R.J., Choi D.W. 2000a. L-type Ca2+ channel-mediated Zn2+ toxicity and modulation by ZnT-1 in PC12 cells. Brain Res. 886:99–107
Kim D. 2005. Physiology and pharmacology of two-pore domain potassium channels. CurLPhanripes. 11:2717–2736
Kim J.A., Kang Y.S., Jung M.W., Kang G.H., Lee S.H., Lee Y.S. 2000b. Ca2+ influx mediates apoptosis induced by 4-aminopyridine, a K+ channel blocker, m HepG2 human hepatoblastoma cells. Pharmacology 60:74–81
Kim J.A., Kang Y.S., Jung M.W., Lee S.H., Lee Y.S. 1999. Involvement of Ca2+ influx in the mechanism of tamoxifen-induced apoptosis in HepG2 human hepatoblastoma cells. Cancer Lett 147:115–123
Kim J.A., Kang Y.S., Lee Y.S. 2003. Role of Ca2+ activated Cl− channels in the mechanism of apoptosis induced by cyclosporin A in a human hepatoma cell line. Biochem. Biophys. Res. Commun. 309:291–297
Kobayashi T., Mori Y. 1998. Ca2+ channel antagonists and neuroprotection from cerebral ischemia. Eur. J. Pharmacol. 363:1–15
Koike T., Ninomiya T. 2000. Alteration of veratridine neurotoxicity in sympathetic neurons during development in vitro. Neuroreport 11:151–155
Koike T., Tanaka S., Oda T., Ninomiya T. 2000. Sodium overload through voltage-dependent Na+ channels induces necrosis and apoptosis of rat superior cervical ganglion cells in vitro, Brain Res. Bull. 51:345–355
Kumar A.R., Kurup P.A. 2002. Inhibition of membrane Na+-K+ ATPase activity: a common pathway in central nervous system disorders. J. Assoc. Physicians India 50:400–406
Kurosawa M., Tani Y., Nishimura S., Numazawa S., Yoshida T. 2001. Distinct PKC isozymes regulate bufalin-induced differentiation and apoptosis in human monocytic cells. Am. J. Physiol. 280:C459–464
Lang F., Lang K.S., Wieder T., Myssina S., Birka C., Lang PA, Kaiser S., Kempe D., Duranton C., Huber S.M. 2003a. Cation channels, cell volume and the death of an erythrocyte. Pfluegers Arch. 447:121–125
Lang F., Lang P.A., Lang K.S., Brand V., Tanneur V., Duranton C., Wieder T., Huber S.M. 2004a. Channel-induced apoptosis of infected host cells-the case of malaria. Pfluegers Arch. 448:319–324
Lang H., Schulte B.A., Schmiedt R.A. 2005. Ouabain induces apoptotic cell death in type I spiral ganglion neurons, but not type II neurons. J. Assoc. Res. Otolaryngol. 6:63–74
Lang K.S., Duranton C., Poehlmann H., Myssina S., Bauer C., Lang F., Wieder T., Huber S.M. 2003b. Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ. 10:249–256
Lang K.S., Myssina S., Brand V., Sandu C., Lang P.A., Berchtold S., Huber S.M., Lang F., Wieder T. 2004b. Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ. 11:231–243
Lang K.S., Myssina S., Lang P.A., Tanneur V., Kempe D.S., Mack A.F., Huber S.M., Wieder T., Lang F., Duranton C. 2004c. Inhibition of erythrocyte phosphatidylserine exposure by urea and Cl. Am. J. Physiol. 286:F1046–1053
Lang K.S., Myssina S., Tanneur V., Wieder T., Huber S.M., Lang F., Duranton C. 2003c. Inhibition of erythrocyte cation channels and apoptosis by ethylisopropylamiloride. Naunyn Schmiedebergs Arch. Pharmacol. 367:391–396
Lang PA., Kaiser S., Myssina S., Wieder T., Lang F., Huber S.M. 2003d. Role of Ca2+ activated K+ channels in human erythrocyte apoptosis. Am. J. Physiol. 285:C1553–1560
Lauritzen I., Zanzouri M., Honore E., Duprat F., Ehrengruber M.U., Lazdunski M., Patel A.J. 2003. K+ Independent cerebellar granule neuron apoptosis. Role of task leak K+ channels. J. Biol. Chem. 278:32068–32076
Lee Y.S. 2004. Mechanism of apoptosis induced by diazoxide, a K+ channel opener, in HepG2 human hepatoma cells. Arch. Pharm. Res. 27:305–313
Lees G.J. 1991. Inhibition of sodium-potassium-ATPase: a potentially ubiquitous mechanism contributing to central nervous system neuropathology. Brain Res. Rev. 16:283–300
Lehotsky J., Kaplan P., Murin R., Raeymaekers L. 2002. The role of plasma membrane Ca+ pumps (PMCAs) in pathologies of mammalians cells. Front. Biosci. 7:d53–84.
Lewis J.M., Truong T.N., Schwartz M.A. 2002. Integrins regulate the apoptotic response to DNA damage through modulation of p53. Proc. Natl. Acad. Sci. USA 99:3627–3632
Ma Z.G., Wang J., Jiang H., Xie J.X., Chen L. 2005. C31 enhances voltage-gated calcium channel currents in undifferentiated PC12 cells. Neurosci. Lett 382:102–105
MacManus A., Ramsden M., Murray M., Henderson Z., Pearson H.A., Campbell V.A. 2000. Enhancement of (45) Ca2+ influx and voltage-dependent Ca2+ channel activity by beta-amyloid-(1-40) in rat cortical synaptosomes and cultured cortical neurons. Modulation by the proinflammatory cytokine interleukin-1beta. J. Bio. Chem. 275:4713–4718
Maeno E., Ishizaki Y., Kanaseki T., Hazama A., Okada Y. 2000. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. USA 97:9487–9492
Manion M.K., Su Z., Villain M., Blalock J.E. 2000. A new type of Ca2+ channel blocker that targets Ca2+ sensors and prevents Ca2+ mediated apoptosis: Faseb J. 14:1297–1306
Mann C.L., Bortner C.D., Jewell C.M., Cidlowski J.A. 2001. Glucocorticoid-induced plasma membrane depolarization during thymocyte apoptosis: association with cell shrinkage and degradation of the Na+/K+-adenosine triphosphatase. Endocrinology 142: 5059–5068
Mann C.L., Cidlowski J.A. 2001. Glucocorticoids regulate plasma membrane potential during rat thymocyte apoptosis in vivo and in vitro. Endocrinology 142:421–429
Mason D.T., Zelis R., Lee G., Hughes J.L., Spann J.F., Jr., Amsterdam E.A. 1971. Current concepts and treatment of digitalis toxicity. Am. J. Cardiol. 27:546–559
Mason R.P., Leeds P.R., Jacob R.F., Hough C.J., Zhang K.G., Mason P.E., Chuang D.M. 1999. Inhibition of excessive neuronal apoptosis by the calcium antagonist amlodipine and antioxidants in cerebellar granule cells. J. Neurochem. 72:1448–1456
McConkey D.J., Lin Y., Nutt L.K., Ozel H.Z., Newman R.A. 2000. Cardiac glycosides stimulate Ca2+ increases and apoptosis in androgen-independent, metastatic human prostate adenocarcinoma cells. Cancer Res. 60:3807–3812
Mehta A., Shaha C. 2004. Apoptotic death in Leishmania donovani promastigotes in response to respiratory chain inhibition: complex II inhibition results in increased pentamidine cytotoxicity. J. Biol. Chem. 279:11798–11813
Meng X.J., Carruth M.W., Weinman S. 1997. Leukotriene D4 activates a chloride conductance in hepatocytes from lipopolysaccharide-treated rats. J. Clin. Invest. 99:2915–2922
Migheli A., Piva R., Casolino S., Atzori C., Dlouhy S.R., Ghetti B. 1999. A cell cycle alteration precedes apoptosis of granule cell precursors in the weaver mouse cerebellum. Am. J. Pathol. 155:365–373
Miller R.J. 2001. Rocking and rolling with Ca2+ channels. Trends Neurosci. 24:445–449
Mishra O.P., Delivoria-Papadopoulos M. 1999. Cellular mechanisms of hypoxic injury in the developing brain. Brain Res. Bull. 48:233–238
Mizoguchi K., Maeta H., Yamamoto A., Oe M., Kosaka H. 2002. Amelioration of myocardial global ischemia/reperfusion injury with volume-regulatory chloride channel inhibitors in vivo. Transplantation 73:1185–1193
Mukherjee S.B., Das M., Sudhandiran G., Shaha C. 2002. Increase in cytosolic Ca2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J. Biol. Chem. 277:24717–24727
Murata Y., Iwasaki H., Sasaki M., Inaba K., Okamura Y. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature. 435:1239–1243
Myssina S., Lang P.A., Kempe D.S., Kaiser S., Huber S.M., Wieder T., Lang F. 2004. Clythannel blockers NPPB and niflumic acid blunt Ca2+-induced erythrocyte ‘apoptosis’. Cell Physiol. Biochem. 14:241–248
Nam J.H., Yoon S.S., Kirn T.J., Uhm D.Y., Kirn S.J. 2003. Slow and persistent increase of [Ca2+]c in response to ligation of surface IgM in WEHI-231 cells. FEBSLett 535:113–118
Nicotera P., Melino G. 2004. Regulation of the apoptosis-necrosis switch. Oncogene, 23:2757–2765
Nietsch H.H., Roe M.W., Fiekers J.F., Moore A.L., Lidofsky S.D. 2000. Activation of potassium and chloride channels by tumor necrosis factor alpha. Role in liver cell death. J. Biol. Chem. 275:20556–20561
Nilius B., Droogmans G. 2003. Amazing chloride channels: an overview. Acta Physiol. Scand 177:119–147
Nobel C.S., Aronson J.K., Dobbelsteen D.J., Slater A.F. 2000. Inhibition of Na+/K+-ATPase may be one mechanism contributing to potassium efflux and cell shrinkage in CD95-induced apoptosis. Apoptosis 5:153–163
Nolte F., Friedrich O., Rojewski M., Fink R.H., Schrezenmeier H., Korper S. 2004. Depolarisation of the plasma membrane in the arsenic trioxide (As2O3)-and anti-CD95-induced apoptosis in myeloid cells. FEBS Lett. 578:85–89
Nowak G. 2002. Protein kinase C-alpha and ERK1/2 mediate mitochondrial dysfunction, decreases in active Na+ transport, and cisplatin-induced apoptosis in renal cells. J. Biol. Chem. 277:43377–43388
Nutt L.K., Margolis S.S., Jensen M., Herman C.E., Dunphy W.G., Rathmell J.C., Kornbluth S. 2005. Metabolic regulation of oocyte cell death through the CaMKII-mediated phosphorylation of caspase-2. Cell 123:89–103
Okada Y., Maeno E. 2001. Apoptosis, cell volume regulation and volume-regulatory chloride channels. Comp Biochem Physiol A Mol Integr Physiol. 130:377–383
Okada Y., Maeno E., Shimizu T., Manabe K., Mori S., Nabekura T. 2004. Dual roles of plasmalemmal chloride channels in induction of cell death. Pfluegers Arch. 448:287–295
Olej B., dos Santos N.F., Leal L, Rumjanek V.M. 1998. Ouabain induces apoptosis on PHA-activated lymphocytes. Biosci Rep. 18:1–7
Olivotto M., Arcangeli A., Carla M., Wanke E. 1996. Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. Bioessays. 18:495–504
Omar A.I., Senatorov V.V., Hu B. 2000. Ethidium bromide staining reveals rapid cell dispersion in the rat dentate gyrus following ouabain-induced injury. Neuroscience. 95:73–80
Orlov S.N., Dam T.V., Tremblay J., Hamet P. 1996. Apoptosis in vascular smooth muscle cells: role of cell shrinkage. Biochem. Biophys. Res. Commun. 221:708–715
Orlov S.N., Pchejetski D.V., Sarkissian S.D., Adarichev V., Taurin S., Pshezhetsky A.V., Tremblay J., Maximov G.V., deBlois D., Bennett M.R., Hamet P., 2003. [3H]-thymidine labelling of DMA triggers apoptosis potentiated by E1 A-adenoviral protein. Apoptosis. 8:199–208
Orrenius S., Zhivotovsky B., Nicotera P. 2003. Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4:552–565
Otori Y, Kusaka S., Kawasaki A., Morimura H., Miki A., Tano Y. 2003. Protective effect of nilvadipine against glutamate neurotoxicity in purified retinal ganglion cells. Brain Res. 961:213–219
Parekh A.B., Putney J.W., Jr. 2005. Store-operated calcium channels. Physiol Rev. 85:757–810
Paszty K., Verma A.K., Padanyi R., Filoteo A.G., Penniston J.T., Enyedi A. 2002. Plasma membrane Ca2+ ATPase isoform 4b is cleaved and activated by caspase-3 during the early phase of apoptosis. J. Biol. Chem. 277:6822–6829
Patrick J., Hilton P.J. 1979. Characterization of sodium-transport disorders in disease: different effects upon sodium and potassium of changes in the sodium pump and in membrane permeability. Clin. Sci. (Lond). 57:289–293
Peluso J.J. 2003. Basic fibroblast growth factor (bFGF) regulation of the plasma membrane calcium ATPase (PMCA) as part of an anti-apoptotic mechanism of action. Biochem. Pharmacol. 66:1363–1369
Penning L.C., Denecker G., Vercammen D., Declercq W., Schipper R.G., Vandenabeele P. 2000. A role for potassium in TNF-induced apoptosis and gene-induction in human and rodent tumour cell lines. Cytokine 12:747–750
Pigozzi D., Tombal B., Ducret T., Vacher P., Gailly P. 2004. Role of store-dependent influx of Ca2+ and efflux of K+ in apoptosis of CHO cells. Cell Calcium 36:421–430
Porcelli A.M., Ghelli A., Zanna C., Valente P., Ferroni S., Rugolo M. 2003. Staurosporine induces apoptotic volume decrease (AVD) in ECV304 cells. Am. N. Y. Acad. Sci. 1010:342–346
Porcelli A.M., Ghelli A., Zanna C., Valente P., Ferroni S., Rugolo M. 2004. Apoptosis induced by Staurosporine in ECV304 cells requires cell shrinkage and upregulation of Cl- conductance. Cell Death Differ. 11:655–662
Putney J.W. 2005. Physiological mechanisms of TRPC activation. Pflugers Arch. 451:29–34
Rasola A., Farahi Far D., Hofman P., Rossi B. 1999. Lack of internucleosomal DMA fragmentation is related to Cl− efflux impairment in hematopoietic cell apoptosis. FASEB. 13:1711–1723
Read D.S., McCall M.A., Gregg R.G. 2002. Absence of voltage-dependent calcium channels delays photoreceptor degeneration in rd mice. Exp Eye Res. 75:415–420
Remillard C.V., Yuan J.X. 2004. Activation of K+ channels: an essential pathway in programmed cell death. Am. J. Physiol. 286:L49–67
Rizzuto R., Pinton P., Ferrari D., Chami M., Szabadkai G., Magalhaes P.J., Di Virgilio F., Pozzan T. 2003. Calcium and apoptosis: facts and hypotheses. Oncogenel 22:8619–8627
Rodrigo R., Trujillo S., Bosco C., Orellana M., Thielemann L., Araya J. 2002. Changes in (Na + K)-adenosine triphosphatase activity and ultrastructure of lung and kidney associated with oxidative stress induced by acute ethanol intoxication. Chest 121:589–596
Ronquist G., Waldenstrom A. 2003. Imbalance of plasma membrane ion leak and pump relationship as a new aetiological basis of certain disease states. J. Intern. Med. 254:517–526
Rose A.M., Valdes R., Jr. 1994. Understanding the sodium pump and its relevance to disease, Clin. Chem. 40:1674–1685
Rozental R., Faharani R., Yu Y., Johnson J.M., Chan S.O., Chiu F.C. 2004. Sodium butyrate induces apoptosis in MSN neuroblastoma cells in a calcium independent pathway. Neurochem. Res. 29:2125–2134
Sano Y., Inamura K., Miyake A., Mochizuki S., Yokoi H., Matsushime H., Furuichi K. 2001. Immunocyte Ca2+ influx system mediated by LTRPC2. Science. 293:1327–1330
Sasamura S., Furukawa K., Shiratori M., Motomura S., Ohizumi Y. 2002. Antisense-inhibition of plasma membrane Ca2+ pump induces apoptosis in vascular smooth muscle cells. Jpn. J. Pharmacol. 90:164–172
Schmiedt R.A., Okamura H.O., Lang H., Schulte B.A. 2002. Ouabain application to the round window of the gerbil cochlea: a model of auditory neuropathy and apoptosis. J. Assoc. Res. Otolaryngol. 3:223–233
Schumann M.A., Gardner P., Raffin T.A. 1993. Recombinant human tumor necrosis factor alpha induces calcium oscillation and calcium-activated chloride current in human neutrophils. The role of calcium/calmodulin-dependent protein kinase. J. Biol. Chem. 268:2134–2140
Schwab B.L, Guerini D., Didszun C., Bano D., Ferrando-May E., Fava E., Tarn J., Xu D., Xanthoudakis S., Nicholson D.W., Carafoli E., Nicotera P. 2002. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ. 9:818–831
Scoltock A.B., Bortner C.D., St J.B.G., Putney J.W., Jr., Cidlowski J.A. 2000, A selective requirement for elevated calcium in DMA degradation, but not early events in anti-Fas-induced apoptosis, J. Biol. Chem. 275:30586–30596
Scoltock A.B., Cidlowski J.A.. 2004. Activation of intrinsic and extrinsic pathways in apoptotic signaling during UV-C-induced death of Jurkat cells: the role of caspase inhibition. Exp. Cell Res. 297:212–223
Sen N., Das B.B., Ganguly A., Mukherjee T., Bandyopadhyay S., Majumder H.K. 2004. Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. J. Biol. Chem. 279:52366–52375
Shimizu T., Numata T., Okada Y. 2004. A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl(-) channel. Proc. Natl. Acad. Sci USA 101:6770–6773
Small D.L, Morley P., Buchan A.M. 1999. Biology of ischemic cerebral cell death. Prog. Cardiovasc. Dis. 42:185–207
Small D.L., Tauskela J., Xia Z. 2002. Role for chloride but not potassium channels in apoptosis in primary rat cortical cultures. Neurosci. Lett. 334:95–98
Sook Han M., Shin K.J., Kim Y.H, Kim S.H, Lee T., Kim E., Ho Ryu S., Suh P.G. 2003. Thiram and ziram stimulate non-selective cation channel and induce apoptosis in PC12 cells. Neurotoxicology. 24:425–434
Souktani R., Berdeaux A., Ghaleh B., Giudicelli J.F., Guize L., Le Heuzey J.Y., Henry P. 2000. Induction of apoptosis using sphingolipids activates a chloride current in Xenopus laevis oocytes. Am. J. Physiol. 279:C158–165
Stelmashook E.V., Weih M., Zorov D., Victorov I., DirnagI U., Isaev N. 1999. Short-term block of Na+/K+-ATPase in neuro-glial cell cultures of cerebellum induces glutamate dependent damage of granule cells. FEBS Lett 456:41–44
Storey N.M., Gomez-Angelats M., Bortner C.D., Armstrong D.L., Cidlowski J.A. 2003. Stimulation of Kv1.3 potassium channels by death receptors during apoptosis in Jurkat T lymphocytes. J. Biol. Chem. 278:33319–33326
Sudhandiran G., Shaha C. 2003. Antimonial-induced increase in intracellular Ca2+ through non-selective cation channels in the host and the parasite is responsible for apoptosis of intracellular Leishmania donovani amastigotes. J. Biol. Chem. 278:25120–25132
Svoboda K.R., Linares A.E., Ribera A.B. 2001. Activity regulates programmed cell death of zebrafish Rohon-Beard neurons. Development 128:3511–3520
Szabo I., Lepple-Wienhues A., Kaba K.N., Zoratti M., Gulbins E., Lang F. 1998. Tyrosine kinase-dependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. Proc. Natl. Acad. Sci. USA 95:6169–6174
Szaszi K., Sirokmany G., Di Ciano-Oliveira C., Rotstein O.D., Kapus A. 2005. Depolarization induces Rho-Rho kinase-mediated myosin light chain phosphorylation in kidney tubular cells. Am. J. Physiol. 289:C673–685
Takahashi N., Wang X., Tanabe S., Uramoto H., Jishage K., Uchida S., Sasaki S., Okada Y. 2005. CIC-3-independent sensitivity of apoptosis to Cl− channel blockers in mouse cardiomyocytes. Cell Physiol. Biochem. 15:263–270
Tanabe S., Wang X., Takahashi N., Uramoto H., Okada Y. 2005. HCO -3 /– independent rescue from apoptosis by stilbene derivatives in rat cardiomyocytes. FEBS Lett. 579:517–522
Tanaka T., Nangaku M., Miyata T., Inagi R., Ohse T., Ingelfinger J.R., Fujita T. 2004. Blockade of calcium influx through L-type calcium channels attenuates mitochondrial injury and apoptosis in hypoxic renal tubular cells. J. Am. Soc. Nephrol. 15:2320–2333
Tang M.J., Cheng Y.R., Lin H.H. 1996. Role of apoptosis in growth and differentiation of proximal tubule cells in primary cultures. Biocherm. Biophys. Res. Commun. 218:658–664
Tapia-Vieyra J.V., Mas-Oliva J. 2001. Apoptosis and cell death channels in prostate cancer. Arch. Med. Res. 32:175–185
Taylor C.P., Meldrum B.S. 1995. Na+ channels as targets for neuroprotective drugs. Trends Pharmacol. Sci. 16:309–316
Thevenod F., Friedmann J.M. 1999. Cadmium-mediated oxidative stress in kidney proximal tubule cells induces degradation of Na+/K+-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEB J. 13:1751–1761
Thompson G.J., Langlais C., Cain K., Conley E.G., Cohen G.M. 2001. Elevated extracellular K+ inhibits death-receptor- and chemical-mediated apoptosis prior to caspase activation and cytochrome c release. Biochem. J. 357:137–145
Tombal B., Denmeade S.R., Isaacs J.T. 1999. Assessment and validation of a microinjection method for kinetic analysis of [Ca2+]i in individual cells undergoing apoptosis. Cell Calcium 25:19–28
Tsukimoto M., Harada H., Ikari A., Takagi K. 2005. Involvement of chloride in apoptotic cell death induced by activation of ATP-sensitive P2X7 purinoceptor. J. Biol. Chem. 280:2653–2658
Uhlemann A.C, Muller C,, Madlung J., Gulbins E., Lang F., 2000. Inhibition of CD95/Fas-induced DMA degradation by osmotic cell shrinkage. Cell. Physiol. Biochem. 10:219–228
Ulbricht W. 1998. Effects of veratridine on sodium currents and fluxes. Rev. Biochem. Pharmacol. 133:1–54
Vanden Abeele F, Skryma R, Shuba Y, Van Coppenolle F, Slomianny C, Roudbaraki M, Mauroy B, Wuytack F, Prevarskaya N. 2002. Bcl-2-dependent modulation of Ca2+ homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 1:169–179
Vereninov A.A, Goriachaia T.S, Matveev V.V, Moshkov A.V, Rozanov lu M, Sakuta G.A, Shirokova A.V, lurinskaia V.E. 2004. [Cell shrinkage during apoptosis is not obligatory. Apoptosis of U937 cells induced by staurosporine and etoposide]. Tsitologiia 46:609–619
Verheye-Dua FA, Bohm L. 2000. Influence of apoptosis on the enhancement of radiotoxicity by ouabain. Strahlenther. Onkol. 176:186–191
Voets T., Nilius B. 2003. TRPs make sense. J. Membrane. Biol. 192:1–8
Wang L, Bhattacharjee A., Zuo Z, Hu F., Honkanen R.E., Berggren P.O., Li M. 1999. A low voltage-activated Ca2+ current mediates cytokine-induced pancreatic beta-cell death. Endocrinology 140: 1200–1204
Wang X.Q., Xiao A.Y., Sheline C., Hyrc K., Yang A., Goldberg M.P., Choi D.W., Yu S.P. 2003a. Apoptotic insults impair Na+, K+-ATPase activity as a mechanism of neuronal death mediated by concurrent ATP deficiency and oxidant stress. J.Cell Sci. 116:2099–2110
Wang X.Q., Xiao A.Y., Yang A., LaRose L., Wei L., Yu S.P. 2003b. Block of Na+, K+ ATPase and induction of hybrid death by 4-aminopyridine in cultured cortical neurons. J. Pharmacol. Exp. Ther. 305:502–506
Wang X.Q, Yu S.P. 2005. Novel regulation of Na, K-ATPase by Src tyrosine kinases in cortical neurons. J. Neurochem. 93:1515–1523
Wang Z. 2004. Roles of K+ channels in regulating tumour cell proliferation and apoptosis. Pfluegers Arch. 448:274–286
Waring P. 2005. Redox active calcium ion channels and cell death. Arch Biochem Biophys. 434:33–42
Watabe M, Masuda Y, Nakajo S, Yoshida T, Kuroiwa Y, Nakaya K. 1996. The cooperative interaction of two different signaling pathways in response to bufalin induces apoptosis in human leukemia U937 cells. J. Biol. Chem. 271:14067–14072
Waxman S.G. 2001, Transcriptional channelopathies: an emerging class of disorders. Nat. Rev. Neurosci. 2:652–659
Wehner F., Olsen H., Tinel H., Kinne-Saffran E., Kinne R.K. 2003. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev. Physiol. Biochem. Pharmacol. 148:1–80
Wei L, Xiao A.Y, Jin C, Yang A., Lu Z.Y, Yu S,P. 2004. Effects of chloride and potassium channel blockers on apoptotic cell shrinkage and apoptosis in cortical neurons. Pfluegers Arch. 448:325–334
Williams S.S., French J.N., Gilbert M., Rangaswami A.A., Walleczek J., Knox S.J. 2000. Bcl-2 overexpression results in enhanced capacitative calcium entry and resistance to SKF-96365-induced apoptosis. Cancer Res. 60:4358–4361
Wright S.H. 2004. Generation of resting membrane potential. Ady. Physiol. Educ. 28:139–142
Wu X, Ahn E.Y., McKenna MA, Yeo H., McDonald J.M. 2005. Fas binding to calmodulin regulates apoptosis in osteoclasts. J. Biol. Chem. 280:29964–29970
Xiao A.Y., Wang X.Q., Yang A., Yu S.P. 2002a. Slight impairment of Na+, K+-ATPase synergistically aggravates ceramide- and beta-amyloid-induced apoptosis in cortical neurons. Brain Res. 955:253–259
Xiao A.Y., Wei L, Xia S., Rothman S., Yu S.P. 2002b. Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J. Neurosci. 22:1350–1362
Yagami T., Ueda K., Asakura K., Nakazato H., Hata S., Kuroda T., Sakaeda T., Sakaguchi G., Itoh N., Hashimoto Y., Hori Y. 2003a. Human group IIA secretory phospholipase A2 potentiates Ca2+ influx through L-type voltage- sensitive Ca2+ channels in cultured rat cortical neurons. J. Neurochem. 85:749–758
Yagami T., Ueda K., Asakura K., Okamura N., Sakaeda T., Sakaguchi G., Itoh N., Hashimoto Y., Nakano T., Fujimoto M. 2003b. Effect of Gas6 on secretory phospholipase A(2)-IIA-induced apoptosis in cortical neurons. Brain Res. 985:142–149
Yagami T., Ueda K., Asakura K., Sakaeda T., Hata S., Kuroda T., Sakaguchi G., Itoh N., Hashimoto Y., Hori Y. 2003c. Porcine pancreatic group IB secretory phospholipase A2 potentiates Ca2+ influx through L-type voltage-sensitive Ca2+ channels. Brain Res. 960:71–80
Yagami T., Ueda K., Asakura K., Sakaeda T., Nakazato H., Kuroda T., Hata S., Sakaguchi G., Itoh N., Nakano T., Kambayashi Y., Tsuzuki H. 2002. Gas6 rescues cortical neurons from amyloid beta protein-induced apoptosis. Neuropharmacology 43: 1289–1296
Yagami T., Ueda K., Sakaeda T., Itoh N., Sakaguchi G., Okamura N., Hori Y., Fujimoto M. 2004. Protective effects of a selective L-type voltage-sensitive calcium channel blocker, S-312-d, on neuronal cell death. Biochem. Pharmacol. 67:1153–1165
Yagami T., Ueda K., Sakaeda T., Okamura N., Nakazato H., Kuroda T., Hata S., Sakaguchi G., Itoh N., Hashimoto Y., Fujimoto M. 2005. Effects of an endothelin B receptor agonist on secretory phospholipase A2-IIA-induced apoptosis in cortical neurons. Neuropharmacology 48:291–300
Yoon J., Ben-Ami H.C., Hong Y.S., Park S., Strong L.L., Bowman J., Geng C., Baek K., Minke B., Pak W.L. 2000. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J. Neurosci. 20:649–659
Yu S.P. 2003a. Na+, K+-ATPase: the new face of an old player in pathogenesis and apoptotic/hybrid cell death. Biochem. Pharmacol. 66:1601–1609
Yu S.P. 2003b. Regulation and critical role of potassium homeostasis in apoptosis. Prog. Neurobiol. 70:363–386
Yu S.P., Canzoniero L.M., Choi D.W. 2001. Ion homeostasis and apoptosis. Curr. Opin. Cell Biol. 13:405–411
Yu S.P., Yeh C.H., Sensi S.L, Gwag B.J., Canzoniero L.M., Farhangrazi Z.S., Ying H.S., Tian M., Dugan L.L., Choi D.W. 1997. Mediation of neuronal apoptosis by enhancement of outward potassium current. Science 278:1 14–1 17
Zagranichnaya T.K., Wu X., Danos A.M., Villereal M.L. 2005. Gene expression profiles in HEK-293 cells with low or high store-operated calcium entry: can regulatory as well as regulated genes be identified? Physio. Genomics 21: 14–33
Zamaraeva M.V., Sabirov R.Z., Maeno E., Ando-Akatsuka Y., Bessonova S.V., Okada Y. 2005. Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ. 12:1390–1397
Zhang W., Chu X., long Q., Cheung J.Y., Conrad K., Masker K., Miller B.A. 2003. A novel TRPM2 isoform inhibits calcium influx and susceptibility to cell death. J. Biol. Chem. 278:16222-16229
Zhong J., Deng J., Huang S., Yang X., Lee W.H. 2004. High K+ and IGF-1 protect cerebellar granule neurons via distinct signaling pathways. J. Neurosci. Res. 75:794–806
Zhou J.G., Ren J.L, Qiu Q.Y., He H., Guan Y.Y. 2005. Regulation of intracellular Cl-concentration through volume-regulated CIC-3 chloride channels in A10 vascular smooth muscle cells. J. Biol. Chem. 280:7301–7308
Zhu D.M., Tibbies H.E., Vassilev A.O., Uckun P.M. 2002, SYKand LYN mediate B-cell receptor-independent calcium-induced apoptosis in DT-40 lymphoma B-cells. Leuk. Lymphoma 43:2165–2170
Ziegelhoffer A., Kjeldsen K., Bundgaard H., Breier A., Vrbjar N., Dzurba A. 2000. Na,K-ATPase in the myocardium: molecular principles, functional and clinical aspects. Gen. Physiol. Biophys. 19:9–47
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We appreciate the input of Dr. James W. Jr. Putney.
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Franco, R., Bortner, C. & Cidlowski, J. Potential Roles of Electrogenic Ion Transport and Plasma Membrane Depolarization in Apoptosis. J Membrane Biol 209, 43–58 (2006). https://doi.org/10.1007/s00232-005-0837-5
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DOI: https://doi.org/10.1007/s00232-005-0837-5