Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy.

Inhibition of mitochondrial oxidative phosphorylation progresses to uncoupling when opening of cyclosporin A-sensitive permeability transition pores increases permeability of the mitochondrial inner membrane to small solutes. Involvement of the mitochondrial permeability transition (MPT) in necrotic and apoptotic cell death is implicated by demonstrations of protection by cyclosporin A against oxidative stress, ischemia/reperfusion, tumor necrosis factor-alpha exposure, Fas ligation, calcium overload, and a variety of toxic chemicals. Confocal microscopy directly visualizes the MPT in single mitochondria within living cells from the translocation of impermeant fluorophores, such as calcein, across the inner membrane. Simultaneously, mitochondria release potential-indicating fluorophores. Subsequently, mitochondria swell, causing outer membrane rupture and release of cytochrome c and other proapoptotic proteins from the intermembrane space. In situ a sequence of decreased NAD(P)H, increased free calcium, and increased reactive oxygen species formation within mitochondria promotes the MPT and subsequent cell death. Necrotic and apoptotic cell death after the MPT depends, in part, on ATP levels. If ATP levels fall profoundly, glycine-sensitive plasma membrane permeabilization and rupture ensue. If ATP levels are partially maintained, apoptosis follows the MPT. The MPT also signals mitochondrial autophagy, a process that may be important in removing damaged mitochondria. Cellular features of necrosis, apoptosis, and autophagy frequently occur together after death signals and toxic stresses. A new term, necrapoptosis, describes such death processes that begin with a common stress or death signal, progress by shared pathways, but culminate in either cell lysis (necrosis) or programmed cellular resorption (apoptosis), depending on modifying factors such as ATP.

[1]  V. E. Mack,et al.  Glycine Protects Hepatocytes from Injury Caused by Anoxia, Cold Ischemia and Mitochondrial Inhibitors, But Not Injury Caused by Calcium Ionophores or Oxidative Stress , 1993, Hepatology.

[2]  J. Hoek,et al.  Functional Consequences of the Sustained or Transient Activation by Bax of the Mitochondrial Permeability Transition Pore* , 1999, The Journal of Biological Chemistry.

[3]  C. Hackenbrock Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[4]  P. Seglen,et al.  Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes , 1990, The Journal of cell biology.

[5]  G. Gores,et al.  Extracellular acidosis delays onset of cell death in ATP-depleted hepatocytes. , 1988, The American journal of physiology.

[6]  B. Trump,et al.  Studies on cellular autophagocytosis. A histochemical study on sequential alterations of mitochondria in the glucagon-induced autophagic vacuoles of rat liver. , 1972, Laboratory investigation; a journal of technical methods and pathology.

[7]  Ruedi Aebersold,et al.  Molecular characterization of mitochondrial apoptosis-inducing factor , 1999, Nature.

[8]  M. E. Hahn,et al.  Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. , 2001, Toxicological sciences : an official journal of the Society of Toxicology.

[9]  K. Kristiansen,et al.  STAUROSPORINE‐INDUCED CELL DEATH IN TETRAHYMENA THERMOPHILA HAS MIXED CHARACTERISTICS OF BOTH APOPTOTIC AND AUTOPHAGIC DEGENERATION , 1998, Cell biology international.

[10]  B. Herman,et al.  Mitochondrial and glycolytic dysfunction in lethal injury to hepatocytes by t-butylhydroperoxide: protection by fructose, cyclosporin A and trifluoperazine. , 1993, The Journal of pharmacology and experimental therapeutics.

[11]  A. Halestrap,et al.  Inhibition of Ca2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. , 1990, The Biochemical journal.

[12]  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.

[13]  W. Cascio,et al.  Hypercapnic acidosis and dimethyl amiloride reduce reperfusion induced cell death in ischaemic ventricular myocardium. , 1995, Cardiovascular research.

[14]  T. Gotow,et al.  An ultrastructural and immunohistochemical study of PC12 cells during apoptosis induced by serum deprivation with special reference to autophagy and lysosomal cathepsins. , 1998, Archives of histology and cytology.

[15]  J C Reed,et al.  Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. , 1998, Science.

[16]  T. Dierks,et al.  The mitochondrial aspartate/glutamate and ADP/ATP carrier switch from obligate counterexchange to unidirectional transport after modification by SH-reagents. , 1990, Biochimica et biophysica acta.

[17]  Guido Kroemer,et al.  Mitochondrial control of cell death , 2000, Nature Medicine.

[18]  A. Tolkovsky,et al.  Autophagy Is Activated by Apoptotic Signalling in Sympathetic Neurons: An Alternative Mechanism of Death Execution , 1999, Molecular and Cellular Neuroscience.

[19]  B. Herman,et al.  Inhibition of Na+/H+ exchange preserves viability, restores mechanical function, and prevents the pH paradox in reperfusion injury to rat neonatal myocytes , 1993, Basic Research in Cardiology.

[20]  C. Dive,et al.  Mitochondrial membrane permeabilisation by Bax/Bak. , 2003, Biochemical and biophysical research communications.

[21]  L. Romer,et al.  Mitochondrial dysfunction and cytoskeletal disruption during chemical hypoxia to cultured rat hepatic sinusoidal endothelial cells: The pH paradox and cytoprotection by glucose, acidotic pH, and glycine , 1998, Hepatology.

[22]  G. Kroemer,et al.  Mitochondrial control of nuclear apoptosis , 1996, The Journal of experimental medicine.

[23]  G. Gores,et al.  Glycine cytoprotection during lethal hepatocellular injury from adenosine triphosphate depletion. , 1992, Gastroenterology.

[24]  G. Kroemer,et al.  Bid acts on the permeability transition pore complex to induce apoptosis , 2000, Oncogene.

[25]  G. Haddad,et al.  Mechanisms of neuronal survival during hypoxia: ATP-sensitive K+ channels. , 1994, Biology of the neonate.

[26]  W. Bursch,et al.  Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. , 1996, Carcinogenesis.

[27]  G. Takemura,et al.  "Apoptotic" myocytes in infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with In situ nick end-labeling. , 1998, Circulation.

[28]  H. Jaeschke Redox considerations in hepatic injury and inflammation. , 2002, Antioxidants & redox signaling.

[29]  P. Nicotera,et al.  Intracellular ATP, a switch in the decision between apoptosis and necrosis. , 1998, Toxicology letters.

[30]  J. Lemasters,et al.  Cell surface changes and enzyme release during hypoxia and reoxygenation in the isolated, perfused rat liver , 1983, The Journal of cell biology.

[31]  R. Krämer,et al.  The Reversible Antiport-Uniport Conversion of the Phosphate Carrier from Yeast Mitochondria Depends on the Presence of a Single Cysteine* , 1997, The Journal of Biological Chemistry.

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

[33]  D. Pfeiffer,et al.  Cyclosporin A-sensitive and insensitive mechanisms produce the permeability transition in mitochondria. , 1989, Biochemical and biophysical research communications.

[34]  S. Nagata,et al.  Lethal effect of the anti-Fas antibody in mice , 1993, Nature.

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

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

[37]  H. Jaeschke,et al.  Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. , 2003, Gastroenterology.

[38]  P. Allen,et al.  Inhibition of autophagy abrogates tumour necrosis factor α induced apoptosis in human T‐lymphoblastic leukaemic cells , 1997, British journal of haematology.

[39]  J C Reed,et al.  Bax directly induces release of cytochrome c from isolated mitochondria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Klingenberg,et al.  Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+. , 1996, Biochemistry.

[41]  C. Schworer,et al.  Quantitative relationship between autophagy and proteolysis during graded amino acid deprivation in perfused rat liver. , 1981, The Journal of biological chemistry.

[42]  M. Crompton,et al.  Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. , 1998, European journal of biochemistry.

[43]  G. Gores,et al.  Dysregulation of Apoptosis as a Mechanism of Liver Disease: An Overview , 1998, Seminars in liver disease.

[44]  K. Orita,et al.  Activation of apoptosis during the reperfusion phase after rat liver ischemia. , 1996, Transplantation proceedings.

[45]  K. Kinnally,et al.  Signal presequences increase mitochondrial permeability and open the multiple conductance channel. , 1999, Archives of biochemistry and biophysics.

[46]  S. Novgorodov,et al.  The Peptide Mastoparan Is a Potent Facilitator of the Mitochondrial Permeability Transition (*) , 1995, The Journal of Biological Chemistry.

[47]  P W Gage,et al.  Hypoxia increases persistent sodium current in rat ventricular myocytes. , 1996, The Journal of physiology.

[48]  M. Crompton,et al.  The involvement of cyclosporin A binding proteins in regulating and uncoupling mitochondrial energy transduction. , 1992, Biochimica et biophysica acta.

[49]  B. Herman,et al.  Contribution of the mitochondrial permeability transition to lethal injury after exposure of hepatocytes to t-butylhydroperoxide. , 1995, The Biochemical journal.

[50]  D. Brenner,et al.  The Mitochondrial Permeability Transition Augments Fas-induced Apoptosis in Mouse Hepatocytes* , 2000, The Journal of Biological Chemistry.

[51]  B. Kraupp,et al.  In situ detection of fragmented dna (tunel assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note , 1995, Hepatology.

[52]  A. Halestrap,et al.  Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. , 1993, Journal of molecular and cellular cardiology.

[53]  G. Gores,et al.  Calcium dependence of bleb formation and cell death in hepatocytes. , 1988, Cell calcium.

[54]  J. Weinberg,et al.  Cytoprotective effects of glycine and glutathione against hypoxic injury to renal tubules. , 1987, The Journal of clinical investigation.

[55]  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.

[56]  D. Vaux,et al.  Sequence as well as functional similarity for DIABLO/Smac and Grim, Reaper and Hid? , 2000, Cell Death and Differentiation.

[57]  P. Seglen,et al.  Amino acid control of autophagic sequestration and protein degradation in isolated rat hepatocytes , 1984, The Journal of cell biology.

[58]  J. Lemasters,et al.  Fructose prevents hypoxic cell death in liver. , 1987, The American journal of physiology.

[59]  C. Trautwein,et al.  The Mitochondrial Permeability Transition Is Required for Tumor Necrosis Factor Alpha-Mediated Apoptosis and Cytochrome c Release , 1998, Molecular and Cellular Biology.

[60]  P. Bernardi,et al.  Mitochondrial transport of cations: channels, exchangers, and permeability transition. , 1999, Physiological reviews.

[61]  M. Zoratti,et al.  The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A. , 1991, The Journal of biological chemistry.

[62]  B. Lardeux,et al.  Amino acid and hormonal control of macromolecular turnover in perfused rat liver. Evidence for selective autophagy. , 1987, The Journal of biological chemistry.

[63]  P. Vandenabeele,et al.  Tumor Necrosis Factor-Induced Cytotoxicity is Not Related to Rates of Mitochondrial Morphological Abnormalities or Autophagy-Changes that can be Mediated by TNFR-I or TNFR-II , 1998, Bioscience reports.

[64]  J. Lemasters,et al.  New, simple models to evaluate zone-specific damage due to hypoxia in the perfused rat liver: time course and effect of nutritional state. , 1986, The Journal of pharmacology and experimental therapeutics.

[65]  Y. Emori,et al.  A cascade of degradative hydrolase activity contributes to hepatocyte necrosis during anoxia. , 1996, The American journal of physiology.

[66]  Xiaodong Wang,et al.  Smac, a Mitochondrial Protein that Promotes Cytochrome c–Dependent Caspase Activation by Eliminating IAP Inhibition , 2000, Cell.

[67]  D. Brenner,et al.  The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. , 1998, Biochimica et biophysica acta.

[68]  A. Farhood,et al.  Mechanism of cell death during warm hepatic ischemia‐reperfusion in rats: Apoptosis or necrosis? , 2001, Hepatology.

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

[70]  B. Herman,et al.  Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. , 1997, The American journal of physiology.

[71]  Y. Akao,et al.  Involvement of ICE family proteases in apoptosis induced by reoxygenation of hypoxic hepatocytes. , 1996, The American journal of physiology.

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

[73]  C. Malloy,et al.  Effects of ischemia on intracellular sodium and phosphates in the in vivo rat liver. , 1996, Journal of applied physiology.

[74]  S. Srinivasula,et al.  Cytochrome c and dATP-Dependent Formation of Apaf-1/Caspase-9 Complex Initiates an Apoptotic Protease Cascade , 1997, Cell.

[75]  J. Cheung,et al.  Effects of metabolic acidosis on viability of cells exposed to anoxia. , 1985, The American journal of physiology.

[76]  G. Gores,et al.  Protection by acidotic pH against anoxic cell killing in perfused rat liver: evidence for a pH paradox , 1991, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[77]  T. Wallimann,et al.  The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition , 1998, BioFactors.

[78]  J. Lemasters,et al.  Glycine blocks opening of a death channel in cultured hepatic sinusoidal endothelial cells during chemical hypoxia , 2001, Cell Death and Differentiation.

[79]  A. Vercesi,et al.  Ca2+-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation. , 1997, Archives of biochemistry and biophysics.

[80]  P. Bernardi,et al.  A mitochondrial perspective on cell death. , 2001, Trends in biochemical sciences.

[81]  B. Herman,et al.  ATP depletion rather than mitochondrial depolarization mediates hepatocyte killing after metabolic inhibition. , 1994, The American journal of physiology.

[82]  G. Gores,et al.  Protection by acidotic pH and fructose against lethal injury to rat hepatocytes from mitochondrial inhibitors, ionophores and oxidant chemicals. , 1990, Biochemical and biophysical research communications.

[83]  D. Andrews,et al.  Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator , 2000, Oncogene.

[84]  J. Weinberg,et al.  Development of porous defects in plasma membranes of adenosine triphosphate-depleted Madin-Darby canine kidney cells and its inhibition by glycine. , 1998, Laboratory investigation; a journal of technical methods and pathology.

[85]  Sherry F. Grissom,et al.  The mitochondrial permeability transition initiates autophagy in rat hepatocytes , 2001, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[86]  B. Halliwell,et al.  Free Radicals and Antioxidants in the Year 2000: A Historical Look to the Future , 2000, Annals of the New York Academy of Sciences.

[87]  A. Vercesi,et al.  The Role of Reactive Oxygen Species in Mitochondrial Permeability Transition , 1997, Bioscience reports.

[88]  Zhaoli Sun,et al.  In vitro interleukin-6 treatment prevents mortality associated with fatty liver transplants in rats. , 2003, Gastroenterology.

[89]  R. Zager,et al.  Physiological pH. Effects on posthypoxic proximal tubular injury. , 1993, Circulation research.

[90]  G. D. Block,et al.  Association of acetaminophen hepatotoxicity with fasting and ethanol use. , 1994, JAMA.

[91]  J. Lemasters,et al.  Contribution of increased mitochondrial free Ca2+ to the mitochondrial permeability transition induced by tert‐butylhydroperoxide in rat hepatocytes , 1999, Hepatology.

[92]  D. K. Kuharsky,et al.  Bid-induced Cytochrome c Release Is Mediated by a Pathway Independent of Mitochondrial Permeability Transition Pore and Bax* , 2000, The Journal of Biological Chemistry.

[93]  T. Billiar,et al.  Nitric oxide prevents tumor necrosis factor α–induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S‐nitrosylation of caspase‐8 , 2000, Hepatology.

[94]  T. Chittenden,et al.  Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[95]  J. Lemasters,et al.  Centrilobular injury following hypoxia in isolated, perfused rat liver. , 1981, Science.

[96]  M. Madesh,et al.  Calcium signaling and apoptosis. , 2003, Biochemical and biophysical research communications.

[97]  M. Peter,et al.  Two CD95 (APO‐1/Fas) signaling pathways , 1998, The EMBO journal.

[98]  B. Herman,et al.  The mitochondrial permeability transition mediates both necrotic and apoptotic death of hepatocytes exposed to Br-A23187. , 1999, Toxicology and applied pharmacology.

[99]  S. Korsmeyer,et al.  Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death , 2001, Science.

[100]  J. Lemasters Cytochrome c: Which way out? , 2001, Hepatology.

[101]  B. Kraupp,et al.  In situ detection of fragmented dna (tunel assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note , 1995, Hepatology.

[102]  D. D. Di Monte,et al.  Relationships between the mitochondrial transmembrane potential, ATP concentration, and cytotoxicity in isolated rat hepatocytes. , 1990, Archives of biochemistry and biophysics.

[103]  T. Wieloch,et al.  Blockade of the Mitochondrial Permeability Transition Pore Diminishes Infarct Size in the Rat after Transient Middle Cerebral Artery Occlusion , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[104]  B. Deurs,et al.  Toxin-induced cell lysis: protection by 3-methyladenine and cycloheximide. , 1992, Experimental cell research.

[105]  Xiaodong Wang,et al.  Induction of Apoptotic Program in Cell-Free Extracts: Requirement for dATP and Cytochrome c , 1996, Cell.

[106]  B. Herman,et al.  Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes. , 1997, American journal of physiology. Cell physiology.