Necrotic volume increase and the early physiology of necrosis.

Whether a lethally injured mammalian cell undergoes necrosis or apoptosis may be determined by the early activation of specific ion channels at the cell surface. Apoptosis requires K+ and Cl- efflux, which leads to cell shrinking, an active phenomenon termed apoptotic volume decrease (AVD). In contrast, necrosis has been shown to require Na+ influx through membrane carriers and more recently through stress-activated non-selective cation channels (NSCCs). These ubiquitous channels are kept dormant in viable cells but become activated upon exposure to free-radicals. The ensuing Na+ influx leads to cell swelling, an active response that may be termed necrotic volume increase (NVI). This review focuses on how AVD and NVI become conflicting forces at the beginning of cell injury, on the events that determine irreversibility and in particular, on the ion fluxes that decide whether a cell is to die by necrosis or by apoptosis.

[1]  F. Lang,et al.  The Diversity of Volume Regulatory Mechanisms , 1998, Cellular Physiology and Biochemistry.

[2]  G. Hahn,et al.  Activation of potassium channels by hypoxia and reoxygenation in the human lung adenocarcinoma cell line A549 , 1993, Journal of cellular physiology.

[3]  S. Orrenius,et al.  Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. , 1994, The Journal of biological chemistry.

[4]  D. Choi,et al.  Mediation of neuronal apoptosis by enhancement of outward potassium current. , 1997, Science.

[5]  S. Oja,et al.  Characteristics of ischemia-induced taurine release in the developing mouse hippocampus , 1999, Neuroscience.

[6]  L. Barros,et al.  Measurement of sugar transport in single living cells , 1999, Pflügers Archiv.

[7]  D. Häussinger,et al.  Endogenous hydroperoxide formation, cell volume and cellular K+ balance in perfused rat liver. , 1993, The Biochemical journal.

[8]  G. Gores,et al.  Intracellular pH during "chemical hypoxia" in cultured rat hepatocytes. Protection by intracellular acidosis against the onset of cell death. , 1989, The Journal of clinical investigation.

[9]  C. Waterfield,et al.  Reduction of liver taurine in rats by beta-alanine treatment increases carbon tetrachloride toxicity. , 1993, Toxicology.

[10]  M. Kirsch,et al.  Ca2+-dependent cytotoxicity of H2O2 in L929 cells: the role of H2O2-induced Na+-influx. , 1998, Free radical biology & medicine.

[11]  G. Bellomo,et al.  Alterations of cell volume regulation in the development of hepatocyte necrosis. , 1999, Experimental cell research.

[12]  C. Bortner,et al.  Absence of volume regulatory mechanisms contributes to the rapid activation of apoptosis in thymocytes. , 1996, The American journal of physiology.

[13]  P. Nicotera,et al.  Intracellular Adenosine Triphosphate (ATP) Concentration: A Switch in the Decision Between Apoptosis and Necrosis , 1997, The Journal of experimental medicine.

[14]  D. Green Apoptotic Pathways Paper Wraps Stone Blunts Scissors , 2000, Cell.

[15]  J. S. McDonald,et al.  Cell Swelling, Blebbing, and Death Are Dependent on ATP Depletion and Independent of Calcium During Chemical Hypoxia in a Glial Cell Line (ROC‐1) , 1992, Journal of neurochemistry.

[16]  S. J. Elliott,et al.  Oxidized glutathione mediates cation channel activation in calf vascular endothelial cells during oxidant stress. , 1996, The Journal of physiology.

[17]  V. Fadok,et al.  Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. , 1998, The Journal of clinical investigation.

[18]  F. Lang,et al.  Physiology of apoptosis. , 2000, American journal of physiology. Renal physiology.

[19]  L. Mandel,et al.  Role of cytosolic Ca in renal tubule damage induced by anoxia. , 1991, The American journal of physiology.

[20]  B. Herman,et al.  Blebbing, free Ca2+ and mitochondrial membrane potential preceding cell death in hepatocytes , 1987, Nature.

[21]  A. Melcher,et al.  Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression , 1998, Nature Medicine.

[22]  S. V. Kotelevtsev,et al.  Inversion of the Intracellular Na+/K+Ratio Blocks Apoptosis in Vascular Smooth Muscle at a Site Upstream of Caspase-3* , 1999, The Journal of Biological Chemistry.

[23]  John J. Lemasters,et al.  Mitochondrial Dysfunction in the Pathogenesis of Necrotic and Apoptotic Cell Death , 1999, Journal of bioenergetics and biomembranes.

[24]  G. Majno,et al.  Apoptosis, oncosis, and necrosis. An overview of cell death. , 1995, The American journal of pathology.

[25]  W. Fiers,et al.  Dual Signaling of the Fas Receptor: Initiation of Both Apoptotic and Necrotic Cell Death Pathways , 1998, The Journal of experimental medicine.

[26]  Y. Tsujimoto,et al.  ATP-dependent steps in apoptotic signal transduction. , 1999, Cancer research.

[27]  T. Risler,et al.  Cellular taurine release triggered by stimulation of the Fas(CD95) receptor in Jurkat lymphocytes , 1998, Pflügers Archiv.

[28]  Jin-Moo Lee,et al.  The changing landscape of ischaemic brain injury mechanisms , 1999, Nature.

[29]  S. Budd,et al.  Mitochondria and neuronal survival. , 2000, Physiological reviews.

[30]  Takahiro Shimizu,et al.  Receptor‐mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD) , 2001, The Journal of physiology.

[31]  S. Bhakdi,et al.  Novel path to apoptosis: small transmembrane pores created by staphylococcal alpha-toxin in T lymphocytes evoke internucleosomal DNA degradation , 1994, Infection and immunity.

[32]  B. Krammer,et al.  Cutting edge: differential effect of apoptotic versus necrotic tumor cells on macrophage antitumor activities. , 1999, Journal of immunology.

[33]  Kevin K. W Wang,et al.  Calpain and caspase: can you tell the difference? , 2000, Trends in Neurosciences.

[34]  C. Bortner,et al.  Caspase Independent/Dependent Regulation of K+, Cell Shrinkage, and Mitochondrial Membrane Potential during Lymphocyte Apoptosis* , 1999, The Journal of Biological Chemistry.

[35]  R. Voll,et al.  Immunosuppressive effects of apoptotic cells , 1997, Nature.

[36]  G. Bellomo,et al.  Alteration of Na+ homeostasis as a critical step in the development of irreversible hepatocyte injury after adenosine triphosphate depletion , 1995, Hepatology.

[37]  F. Lang,et al.  Tyrosine kinase-dependent activation of a chloride channel in CD95-induced apoptosis in T lymphocytes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  H. de Groot,et al.  Decrease of ischemic injury to the isolated perfused rat liver by loop diuretics , 1997, Hepatology.

[39]  J. Kourie,et al.  Interaction of reactive oxygen species with ion transport mechanisms. , 1998, American journal of physiology. Cell physiology.

[40]  B. Herman,et al.  Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: A laser scanning confocal microscopic study , 1995, Hepatology.

[41]  A. Borle,et al.  Chemical hypoxia increases cytosolic Ca2+ and oxygen free radical formation. , 1995, Cell calcium.

[42]  S. Korsmeyer,et al.  Cell Death in Development , 1999, Cell.

[43]  M. Ashford,et al.  Activation of a novel non‐selective cation channel by alloxan and H2O2 in the rat insulin‐secreting cell line CRI‐G1 , 1997, The Journal of physiology.

[44]  D. Choi,et al.  NMDA receptor-mediated K+ efflux and neuronal apoptosis. , 1999, Science.

[45]  S. Lipton,et al.  Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function , 1995, Neuron.

[46]  J. Phillis,et al.  Mechanisms of amino acid release from the isolated anoxic/reperfused rat heart. , 1998, European journal of pharmacology.

[47]  C. Bortner,et al.  A necessary role for cell shrinkage in apoptosis. , 1998, Biochemical pharmacology.

[48]  C. Hetz,et al.  Nonselective cation channels as effectors of free radical–induced rat liver cell necrosis , 2001, Hepatology.

[49]  J. Lemasters V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[50]  S. J. Elliott,et al.  Oxidant stress alters Na+ pump and Na(+)-K(+)-Cl- cotransporter activities in vascular endothelial cells. , 1992, The American journal of physiology.

[51]  W. Frishman,et al.  Sodium Ion/Hydrogen Ion Exchange Inhibition: A New Pharmacologic Approach to Myocardial Ischemia and Reperfusion Injury , 1998, Journal of clinical pharmacology.

[52]  S. Lipton,et al.  Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[53]  P. Herson,et al.  Hydrogen Peroxide Induces Intracellular Calcium Overload by Activation of a Non-selective Cation Channel in an Insulin-secreting Cell Line* , 1999, The Journal of Biological Chemistry.

[54]  S. Orrenius,et al.  Cytosolic‐free Ca2+ and cell killing in hepatoma 1c1c7 cells exposed to chemical anoxia , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[55]  M. Lazdunski,et al.  Disruption of Mitochondrial Respiration Inhibits Volume-Regulated Anion Channels and Provokes Neuronal Cell Swelling , 1998, The Journal of Neuroscience.

[56]  W. Stremmel,et al.  Functional interactions between oxidative stress, membrane Na(+) permeability, and cell volume in rat hepatoma cells. , 2000, Gastroenterology.

[57]  J. Noordhoek,et al.  Interaction with cellular ATP generating pathways mediates menadione-induced cytotoxicity in isolated rat hepatocytes. , 1990, Archives of biochemistry and biophysics.

[58]  P. Maher,et al.  Oxidative Stress Induces a Form of Programmed Cell Death with Characteristics of Both Apoptosis and Necrosis in Neuronal Cells , 1998, Journal of neurochemistry.

[59]  S. Orlov,et al.  Inversion of the intracellular Na(+)/K(+) ratio blocks apoptosis in vascular smooth muscle cells by induction of RNA synthesis. , 2000, Hypertension.