Methods for the assessment of mitochondrial membrane permeabilization in apoptosis

Reed JC (2002) Apoptosis-based therapies. Nat Rev Drug Discov 1:111–121

Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267:1456–1462

Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257

Kroemer G, El-Deiry WS, Golstein P et al (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12(Suppl 2):1463–1467

Zamzami N, Marchetti P, Castedo M et al (1996) Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett 384:53–57

Kroemer G, Zamzami N, Susin SA (1997) Mitochondrial control of apoptosis. Immunol Today 18:44–51

Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6:513–519

Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629

Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163

Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–1433

Martins LM, Iaccarino I, Tenev T et al (2002) The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J Biol Chem 277:439–444

Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8:613–621

Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42

Verhagen AM, Ekert PG, Pakusch M et al (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43–53

Susin SA, Lorenzo HK, Zamzami N et al (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446

Modjtahedi N, Giordanetto F, Madeo F, Kroemer G (2006) Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 16:264–272

Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95–99

Cain K, Bratton SB, Cohen GM (2002) The Apaf-1 apoptosome: a large caspase-activating complex. Biochimie 84:203–214

Daugas E, Susin SA, Zamzami N et al (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. Faseb J 14:729–739

Vahsen N, Cande C, Dupaigne P et al (2006) Physical interaction of apoptosis-inducing factor with DNA and RNA. Oncogene 25:1763–1774

Scaffidi C, Fulda S, Srinivasan A et al (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17:1675–1687

Wajant H (2002) The Fas signaling pathway: more than a paradigm. Science 296:1635–1636

Mehlen P, Bredesen DE (2004) The dependence receptor hypothesis. Apoptosis 9:37–49

Debatin KM, Krammer PH (2004) Death receptors in chemotherapy and cancer. Oncogene 23:2950–2966

Fuentes-Prior P, Salvesen GS (2004) The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem J 384:201–232

Krammer PH (2000) CD95's deadly mission in the immune system. Nature 407:789–795

Zamzami N, El Hamel C, Maisse C et al (2000) Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 19:6342–6350

Gonzalvez F, Pariselli F, Dupaigne P et al (2005) tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak. Cell Death Differ 12:614–626

Goonesinghe A, Mundy ES, Smith M, Khosravi-Far R, Martinou JC, Esposti MD (2005) Pro-apoptotic Bid induces membrane perturbation by inserting selected lysolipids into the bilayer. Biochem J 387:109–118

Csordas G, Madesh M, Antonsson B, Hajnoczky G (2002) tcBid promotes Ca(2+) signal propagation to the mitochondria: control of Ca(2+) permeation through the outer mitochondrial membrane. EMBO J 21:2198–2206

Green DR, Kroemer G (1998) The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol 8:267–271

Zamzami N, Kroemer G (2003) Apoptosis: mitochondrial membrane permeabilization–the (w)hole story? Curr Biol 13:R71–73

Baines CP, Kaiser RA, Purcell NH et al (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658–662

Nakagawa T, Shimizu S, Watanabe T et al (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434:652–658

Halestrap AP, Brenner C (2003) The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem 10:1507–1525

Marchetti P, Castedo M, Susin SA et al (1996) Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 184:1155–1160

Jacotot E, Ferri KF, El Hamel C et al (2001) Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J Exp Med 193:509–519

Deniaud A, Brenner C, Kroemer G (2004) Mitochondrial membrane permeabilization by HIV-1 Vpr. Mitochondrion 4:223–233

Sabbah EN, Druillennec S, Morellet N, Bouaziz S, Kroemer G, Roques BP (2006) Interaction between the HIV-1 protein Vpr and the adenine nucleotide translocator. Chem Biol Drug Des 67:145–154

Wei MC, Zong WX, Cheng EH et al (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727–730

Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281–1292

Kuwana T, Mackey MR, Perkins G et al (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331–342

Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ (2001) Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153:1265–1276

Basanez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM, Zimmerberg J (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277:49360–49365

Lucken-Ardjomande S, Martinou JC (2005) Newcomers in the process of mitochondrial permeabilization. J Cell Sci 118:473–483

Garofalo T, Giammarioli AM, Misasi R et al (2005) Lipid microdomains contribute to apoptosis-associated modifications of mitochondria in T cells. Cell Death Differ 12:1378–1389

Banerjee J, Ghosh S (2004) Bax increases the pore size of rat brain mitochondrial voltage-dependent anion channel in the presence of tBid. Biochem Biophys Res Commun 323:310–314

Rostovtseva TK, Antonsson B, Suzuki M, Youle RJ, Colombini M, Bezrukov SM (2004) Bid, but not Bax, regulates VDAC channels. J Biol Chem 279:13575–13583

Brenner C, Grimm S (2006) The permeability transition pore complex in cancer cell death. Oncogene 25:4744–4756

Mitchell P, Moyle J (1965) Evidence discriminating between the chemical and the chemiosmotic mechanisms of electron transport phosphorylation. Nature 208:1205–1206

Mitchell P, Moyle J (1965) Stoichiometry of proton translocation through the respiratory chain and adenosine triphosphatase systems of rat liver mitochondria. Nature 208:147–151

Zamzami N, Larochette N, Kroemer G (2005) Mitochondrial permeability transition in apoptosis and necrosis. Cell Death Differ 12(Suppl 2):1478–1480

Zoratti M, Szabo I, De Marchi U (2005) Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706:40–52

Crompton M, Barksby E, Johnson N, Capano M (2002) Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie 84:143–152

Petronilli V, Miotto G, Canton M et al (1999) Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J 76:725–734

Shimizu S, Ide T, Yanagida T, Tsujimoto Y (2000) Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J Biol Chem 275:12321–12325

Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483–487

Vander Heiden MG, Chandel NS, Li XX, Schumacker PT, Colombini M, Thompson CB (2000) Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc Natl Acad Sci USA 97:4666–4671

Vander Heiden MG, Chandel NS, Schumacker PT, Thompson CB (1999) Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol Cell 3:159–167

Rostovtseva TK, Tan WMC (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37:129–142

Loeffler M, Daugas E, Susin SA et al (2001) Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor. Faseb J 15:758–767

Zhivotovsky B, Orrenius S, Brustugun O, Doskeland S (1998) Injected cytochrome c induces apoptosis. Nature 391:449–450

Adrain C, Creagh EM, Martin SJ (2001) Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J 20:6627–6636

Patterson SD, Spahr CS, Daugas E et al (2000) Mass spectrometric identification of proteins released from mitochondria undergoing permeability transition. Cell Death Differ 7:137–144

Kohler C, Gahm A, Noma T, Nakazawa A, Orrenius S, Zhivotovsky B (1999) Release of adenylate kinase 2 from the mitochondrial intermembrane space during apoptosis. FEBS Letters 447:10–12

Susin SA, Lorenzo HK, Zamzami N et al (1999) Mitochondrial release of caspase-2 and -9 during the apoptotic process. J Exp Med 189:381–394

Anantharam V, Kitazawa M, Wagner J, Kaul S, Kanthasamy AG (2002) Caspase-3-dependent proteolytic cleavage of protein kinase Cdelta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl. J Neurosci 22:1738–1751

van de Donk NW, Kamphuis MM, van Kessel B, Lokhorst HM, Bloem AC (2003) Inhibition of protein geranylgeranylation induces apoptosis in myeloma plasma cells by reducing Mcl-1 protein levels. Blood 102:3354–3362

Campos CB, Paim BA, Cosso RG, Castilho RF, Rottenberg H, Vercesi AE (2006) Method for monitoring of mitochondrial cytochrome c release during cell death: immunodetection of cytochrome c by flow cytometry after selective permeabilization of the plasma membrane. Cytometry A 69:515–523

Goldstein J, Waterhouse N, Juin P, Evan G, Green D (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat Cell Biol 2:156–162

Feldmann G, Haouzi D, Moreau A et al (2000) Opening of the mitochondrial permeability transition pore causes matrix expansion and outer membrane rupture in Fas-mediated hepatic apoptosis in mice. Hepatology 31:674–683

Terauchia S, Yamamotoa T, Yamashita K, Kataoka M, Terada H, Shinohara Y (2005) Molecular basis of morphological changes in mitochondrial membrane accompanying induction of permeability transition, as revealed by immuno-electron microscopy. Mitochondrion 5:248–254

Crouser ED, Gadd ME, Julian MW et al (2003) Quantitation of cytochrome c release from rat liver mitochondria. Anal Biochem 317:67–75

Mootha VK, Wei MC, Buttle KF et al (2001) A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J 20:661–671

Safiulina D, Kaasik A, Seppet E, Peet N, Zharkovsky A, Seppet E (2004) Method for in situ detection of the mitochondrial function in neurons. J Neurosci Methods 137:87–95

Castedo M, Ferri K, Roumier T, Metivier D, Zamzami N, Kroemer G (2002) Quantitation of mitochondrial alterations associated with apoptosis. J Immunol Meth 265:39–47

Metivier D, Dallaporta B, Zamzami N et al (1998) Cytofluorometric detection of mitochondrial alterations in early CD95/Fas/APO-1-triggered apoptosis of Jurkat T lymphoma cells. Comparison of seven mitochondrion-specific fluorochromes. Immunol Lett 61:157–163

Johnson LV, Walsh ML, Chen LB (1980) Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci USA 77:990–994

Schneckenburger H, Stock K, Lyttek M, Strauss WS, Sailer R (2004) Fluorescence lifetime imaging (FLIM) of rhodamine 123 in living cells. Photochem Photobiol Sci 3:127–131

Modica-Napolitano JS, Aprille JR (1987) Basis for the selective cytotoxicity of rhodamine 123. Cancer Res 47:4361–4365

Modica-Napolitano JS, Weiss MJ, Chen LB, Aprille JR (1984) Rhodamine 123 inhibits bioenergetic function in isolated rat liver mitochondria. Biochem Biophys Res Commun 118:717–723

Scaduto RC Jr, Grotyohann LW (1999) Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 76:469–477

Blattner JR, He L, Lemasters JJ (2001) Screening assays for the mitochondrial permeability transition using a fluorescence multiwell plate reader. Anal Biochem 295:220–226

Macho A, Decaudin D, Castedo M et al (1996) Chloromethyl-X-Rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 25:333–340

Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 197:40–45

Reers M, Smith TW, Chen LB (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30:4480–4486

Smiley ST, Reers M, Mottola-Hartshorn C et al (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88:3671–3675

Rottenberg H, Wu S (1998) Quantitative assay by flow cytometry of the mitochondrial membrane potential in intact cells. Biochim Biophys Acta 1404:393–404

Petit PX, Lecoeur H, Zorn E, Dauguet C, Mignotte B, Gougeon ML (1995) Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J Cell Biol 130:157–167

Zamzami N, Marchetti P, Castedo M et al (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367–377

Huser J, Rechenmacher CE, Blatter LA (1998) Imaging the permeability pore transition in single mitochondria. Biophysical Journal 74:2129–2137

Nieminen AL, Byrne AM, Herman B, Lemasters JJ (1997) Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am J Physiol 272:C1286–1294

Poncet D, Boya P, Metivier D, Zamzami N, Kroemer G (2003) Cytofluorometric quantitation of apoptosis-driven inner mitochondrial membrane permeabilization. Apoptosis 8:521–530

Hunter DR, Haworth RA, Southard JH (1976) Relationship between configuration, function, and permeability in calcium-treated mitochondria. J Biol Chem 251:5069–5077

Bernardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F (1999) Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur J Biochem 264:687–701

Lecoeur H, Langonne A, Baux L et al (2004) Real-time flow cytometry analysis of permeability transition in isolated mitochondria. Exp Cell Res 294:106–117

Pouliquen D, Bellot G, Guihard G, Fichet P, Meflah K, Vallette FM (2006) Mitochondrial membrane permeabilization produced by PTP, Bax and apoptosis: a 1H-NMR relaxation study. Cell Death Differ 13:301–310

Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132–1136