Abstract
Apoptosis is important in regulating cell death turnover and is mediated by the intrinsic and death receptor-based extrinsic pathways which converge at the mitochondrial outer membrane (MOM) leading to mitochondrial outer membrane permeabilization (MOMP). MOMP results in the release of apoptotic proteins that further activate the downstream pathway of apoptosis. Thus, tight regulation of MOMP is crucial in controlling apoptosis, and a lack of control may lead to tissue and organ malformation and the development of cancers. Despite a growing number of studies focusing on the structure and activity of the proteins involved in mediating MOMP, such as the Bcl-2 family proteins, the mechanism of MOMP is not well understood. In particular, the crucial role of the various structural properties and changes in lipid components of the MOM in mediating the recruitment and activation of different Bcl-2 proteins remains poorly understood. Furthermore, the factors that control the changes in mitochondrial membrane integrity from the initiation to the final disruption of MOM have yet to be clearly defined. In this review, we provide an overview of studies that focus on the mitochondrial membrane with a biophysical analysis of the interactions of the Bcl-2 proteins with the mitochondrial membrane.
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References
Adams J (2004) The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5:417–421
Andreu-Fernández V, Genoves A, Lee T-H, Stellato M, Lucantoni F, Orzáez M, Mingarro I, Aguilar M-I, Pérez-Payá E (2014) Peptides derived from the transmembrane domain of bcl-2 proteins as potential mitochondrial priming tools. ACS Chem Biol 9:1799–1811
Andreu-Fernandez V, Sancho M, Genoves A, Lucendo E, Todt F, Lauterwasser J, Funk K, Jahreis G, Perez-Paya E, Mingarro I, Edlich F, Orzaez M (2017) Bax transmembrane domain interacts with prosurvival Bcl-2 proteins in biological membranes. Proc Natl Acad of Sci U S A 114:310–315
Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B, Andrews DW (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 24:2096–2103
Ardail D, Privat J, Egret-Charlier M, Levrat C, Lerme F, Louisot P (1990) Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem 265:18797–18802
Ausili A, Torrecillas A, Martínez-Senac MM, Corbalán-García S, Gómez-Fernández JC (2008) The interaction of the Bax C-terminal domain with negatively charged lipids modifies the secondary structure and changes its way of insertion into membranes. J Struct Biol 164:146–152
Ausili A, de Godos A, Torrecillas A, Corbalán-García S, Gómez-Fernández JC (2009) The interaction of the Bax C-terminal domain with membranes is influenced by the presence of negatively charged phospholipids. Biochim Biophysica Acta-Biomembr 1788:1924–1932
Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD (2007) Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 9:550–555
Basanez G, Nechushtan A, Drozhinin O, Chanturiya A, Choe E, Tutt S, Wood K, Hsu Y-T, Zimmerberg J, Youle R (1999) Bax, but not Bcl-xL, decreases the lifetime of planar phospholipid bilayer membranes at subnanomolar concentrations. Proc Natl Acad of Sci U S A 96:5492–5497
Bergelson L, Dyatlovitskaya E, Torkhovskaya T, Sorokina I, Gorkova N (1970) Phospholipid composition of membranes in the tumor cell. Biochim Biophys Acta-lipids and lipid. Metabolism 210:287–298
Bernabeu A, Guillén J, Pérez-Berná AJ, Moreno MR, Villalaín J (2007) Structure of the C-terminal domain of the pro-apoptotic protein Hrk and its interaction with model membranes. Biochim Biophys Acta-Biomembr 1768:1659–1670
Billen LP, Kokoski CL, Lovell JF, Leber B, Andrews DW (2008) Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol 6:e147
Bleicken S, Hofhaus G, Ugarte-Uribe B, Schröder R, García-Sáez A (2016) cBid, Bax and Bcl-xL exhibit opposite membrane remodeling activities. Cell Death Dis 7:e2121
Breckenridge DG, Xue D (2004) Regulation of mitochondrial membrane permeabilization by BCL-2 family proteins and caspases. Curr Opin Cell Biol 16:647–652
Brown JM, Attardi LD (2005) The role of apoptosis in cancer development and treatment response. Nat Rev Cancer 5:231–237
Bürgermeister M, Birner-Grünberger R, Nebauer R, Daum G (2004) Contribution of different pathways to the supply of phosphatidylethanolamine and phosphatidylcholine to mitochondrial membranes of the yeast Saccharomyces Cerevisiae. Biochim Biophys Acta-Mol Cell Biol Lipids 1686:161–168
Certo M, Del Gaizo MV, Nishino M, Wei G, Korsmeyer S, Armstrong SA, Letai A (2006) Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 9:351–365
Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, Huang DC (2005) Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17:393–403
Chen R, Feldstein AE, McIntyre TM (2009) Suppression of mitochondrial function by oxidatively truncated phospholipids is reversible, aided by bid, and suppressed by Bcl-XL. J Biol Chem 284:26297–26308
Chen HC, Kanai M, Inoue-Yamauchi A, Tu HC, Huang Y, Ren D, Kim H, Takeda S, Reyna DE, Chan PM, Ganesan YT, Liao CP, Gavathiotis E, Hsieh JJ, Cheng EH (2015) An interconnected hierarchical model of cell death regulation by the BCL-2 family. Nat Cell Biol 17:1270–1281
Cheng EH-Y, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301:513–517
Chi X, Kale J, Leber B, Andrews DW (2014) Regulating cell death at, on, and in membranes. Biochim Biophys Acta-Mol Cell Res 1843:2100–2113
Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, Green DR (2008) Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad of Sci U S A 105:20327–20332
Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR (2010) The BCL-2 family reunion. Mol Cell 37:299–310
Chipuk JE, McStay GP, Bharti A, Kuwana T, Clarke CJ, Siskind LJ, Obeid LM, Green DR (2012) Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell 148:988–1000
Chou JJ, Li H, Salvesen GS, Yuan J, Wagner G (1999) Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell 96:615–624
Christenson E, Merlin S, Saito M, Schlesinger P (2008) Cholesterol effects on BAX pore activation. J Mol Biol 381:1168–1183
Colbeau A, Nachbaur J, Vignais P (1971) Enzymac characterization and lipid composition of rat liver subcellular membranes. Biochim Biophys Acta-Biomembr 249:462–492
Cosentino K, García-Sáez AJ (2014) Mitochondrial alterations in apoptosis. Chem Phys Lipids 181:62–75
Cosentino K, Garcia-Saez AJ (2017) Bax and Bak pores: are we closing the circle? Trends Cell Biol 27:266–275
Crimi M, Degli Esposti M (2011) Apoptosis-induced changes in mitochondrial lipids. Biochim Biophys Acta-Mol Cell Res 1813:551–557
Czabotar PE, Lee EF, Thompson GV, Wardak AZ, Fairlie WD, Colman PM (2011) Mutation to Bax beyond the BH3 domain disrupts interactions with pro-survival proteins and promotes apoptosis. J Biol Chem 286:7123–7131
Czabotar PE, Lessene G, Strasser A, Adams JM (2014) Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15:49–63
Das KK, Unsay JD, Garcia-Saez AJ (2015) Microscopy of model membranes: understanding how Bcl-2 proteins mediate apoptosis. Adv Planar Lipid Bilayers Liposomes 21:63–97
Degli Esposti M, Cristea I, Gaskell S, Nakao Y, Dive C (2003) Proapoptotic bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Differ 10:1300–1309
Dejean LM, Martinez-Caballero S, Guo L, Hughes C, Teijido O, Ducret T, Ichas F, Korsmeyer SJ, Antonsson B, Jonas EA (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol Biol Cell 16:2424–2432
Dingeldein APG, Pokorná Š, Lidman M, Sparrman T, Šachl R, Hof M, Gröbner G (2017) Apoptotic Bax at Oxidatively stressed mitochondrial membranes: lipid dynamics and Permeabilization. Biophys J 112:2147–2158
Edlich F, Banerjee S, Suzuki M, Cleland MM, Arnoult D, Wang C, Neutzner A, Tjandra N, Youle RJ (2011) Bcl-x L retrotranslocates Bax from the mitochondria into the cytosol. Cell 145:104–116
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516
Eskes R, Desagher S, Antonsson B, Martinou JC (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20:929–935
Fulda S, Debatin K (2006) Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25:4798–4811
Garcea R, Canuto R, Gautero B, Biocca M, Feo F (1980) Phospholipid composition of inner and outer mitochondrial membranes isolated from Yoshida hepatoma AH-130. Cancer Lett 11:133–139
Garcia-Saez A (2012) The secrets of the Bcl-2 family. Cell Death Differ 19:1733–1740
García-Sáez AJ, Buschhorn SB, Keller H, Anderluh G, Simons K, Schwille P (2011) Oligomerization and pore formation by equinatoxin II inhibit endocytosis and lead to plasma membrane reorganization. J Biol Chem 286:37768–37777
Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, Tu H-C, Kim H, Cheng EH-Y, Tjandra N (2008) BAX activation is initiated at a novel interaction site. Nature 455:1076–1081
Gillies LA, Du H, Peters B, Knudson CM, Newmeyer DD, Kuwana T (2015) Visual and functional demonstration of growing Bax-induced pores in mitochondrial outer membranes. Mol Biol Cell 26:339–349
Gloster J, Harris P (1970) The lipid composition of mitochondrial and microsomal fractions from human ventricular myocardium. J Mol Cell Cardiol 1:459–465
Gross A, Yin X-M, Wang K, Wei MC, Jockel J, Milliman C, Erdjument-Bromage H, Tempst P, Korsmeyer SJ (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274:1156–1163
Große L, Wurm CA, Brüser C, Neumann D, Jans DC, Jakobs S (2016) Bax assembles into large ring-like structures remodeling the mitochondrial outer membrane in apoptosis. EMBO J 35:402–413
Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139–150
Horvath SE, Daum G (2013) Lipids of mitochondria. Prog Lipid Res 52:590–614
Hovius R, Lambrechts H, Nicolay K, de Kruijff B (1990) Improved methods to isolate and subfractionate rat liver mitochondria. Lipid composition of the inner and outer membrane. Biochim Biophys Acta-Biomembr 1021:217–226
Ichim G, Tait SW (2016) A fate worse than death: apoptosis as an oncogenic process. Nat Rev Cancer 16:539–548
Jiang Z, Zheng X, Lytle RA, Higashikubo R, Rich KM (2004) Lovastatin-induced up-regulation of the BH3-only protein, Bim, and cell death in glioblastoma cells. J Neurochem 89:168–178
Jourdain A, Martinou J-C (2009) Mitochondrial outer-membrane permeabilization and remodelling in apoptosis. Int J Biochem Cell Biol 41:1884–1889
Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, Osipov AN, Belikova NA, Kapralov AA, Kini V (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1:223–232
Kantari C, Walczak H (2011) Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochim Biophys Acta-Mol Cell Res 1813:558–563
Karch J, Molkentin JD (2014) Identifying the components of the elusive mitochondrial permeability transition pore. Proc Natl Acad of Sci U S A 111:10396–10397
Kaufmann SH, Hengartner MO (2001) Programmed cell death: alive and well in the new millennium. Trends Cell Biol 11:526–534
Kim H, Tu H-C, Ren D, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ-D, Cheng EH-Y (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 36:487–499
Kirkland RA, Adibhatla RM, Hatcher JF, Franklin JL (2002) Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 115:587–602
Kushnareva Y, Andreyev AY, Kuwana T, Newmeyer DD (2012) Bax activation initiates the assembly of a multimeric catalyst that facilitates Bax pore formation in mitochondrial outer membranes. PLoS Biol 10:e1001394
Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, Green DR, Newmeyer DD (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17:525–535
Leber B, Lin J, Andrews DW (2007) Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12:897–911
Leber B, Lin J, Andrews D (2010) Still embedded together binding to membranes regulates Bcl-2 protein interactions. Oncogene 29:5221–5230
Lee EF, Grabow S, Chappaz S, Dewson G, Hockings C, Kluck RM, Debrincat MA, Gray DH, Witkowski MT, Evangelista M (2016) Physiological restraint of Bak by Bcl-xL is essential for cell survival. Genes Dev 30:1240–1250
Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183–192
Li J, Yuan J (2008) Caspases in apoptosis and beyond. Oncogene 27:6194–6206
Lindsay J, Degli Esposti M, Gilmore AP (2011) Bcl-2 proteins and mitochondria—specificity in membrane targeting for death. Biochim Biophys Acta-Mol Cell Res 1813:532–539
Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, Dillon CP, Green DR (2011) A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44:517–531
Lomonosova E, Chinnadurai G (2008) BH3-only proteins in apoptosis and beyond: an overview. Oncogene 27:S2–S19
Lucken-Ardjomande S, Montessuit S, Martinou J-C (2008a) Bax activation and stress-induced apoptosis delayed by the accumulation of cholesterol in mitochondrial membranes. Cell Death Differ 15:484–493
Lucken-Ardjomande S, Montessuit S, Martinou J-C (2008b) Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane. Cell Death Differ 15:929–937
Lutter M, Fang M, Luo X, Nishijima M, Xie X-s, Wang X (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol 2:754–761
Martinou J-C, Youle RJ (2011) Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell 21:92–101
Matsko CM, Hunter OC, Rabinowich H, Lotze MT, Amoscato AA (2001) Mitochondrial lipid alterations during Fas-and radiation-induced apoptosis. Biochem Biophys Res Comm 287:1112–1120
Montero J, Morales A, Llacuna L, Lluis JM, Terrones O, Basañez G, Antonsson B, Prieto J, García-Ruiz C, Colell A (2008) Mitochondrial cholesterol contributes to chemotherapy resistance in hepatocellular carcinoma. Cancer Res 68:5246–5256
Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim DG, Chang BS, Thompson CB, Wong S-L (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381:335–341
Oh KJ, Barbuto S, Meyer N, Kim R-S, Collier RJ, Korsmeyer SJ (2005) Conformational changes in BID, a pro-apoptotic BCL-2 family member, upon membrane binding a SITE-DIRECTED SPIN LABELING STUDY. J Biol Chem 280:753–767
Qin S, Yang C, Li S, Xu C, Zhao Y, Ren H (2012) Smac: its role in apoptosis induction and use in lung cancer diagnosis and treatment. Cancer Lett 318:9–13
Ros U, García-Sáez AJ (2015) More than a pore: the interplay of pore-forming proteins and lipid membranes. J Membr Biol 248:545–561
Rytömaa M, Mustonen P, Kinnunen P (1992) Reversible, nonionic, and pH-dependent association of cytochrome c with cardiolipin-phosphatidylcholine liposomes. J Biol Chem 267:22243–22248
Salvador-Gallego R, Mund M, Cosentino K, Schneider J, Unsay J, Schraermeyer U, Engelhardt J, Ries J, García-Sáez AJ (2016) Bax assembly into rings and arcs in apoptotic mitochondria is linked to membrane pores. EMBO J 35:389–401
Satsoura D, Kučerka N, Shivakumar S, Pencer J, Griffiths C, Leber B, Andrews DW, Katsaras J, Fradin C (2012) Interaction of the full-length Bax protein with biomimetic mitochondrial liposomes: a small-angle neutron scattering and fluorescence study. Biochim Biophys Acta-Biomembr 1818:384–401
Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SB, Chang BS, Minn AJ (1997) Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275:983–986
Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, Du H, Schneiter R, Kuwana T (2009) Mitochondrial outer membrane proteins assist bid in Bax-mediated lipidic pore formation. Mol Biol Cell 20:2276–2285
Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257–288
Shamas-Din A, Brahmbhatt H, Leber B, Andrews DW (2011) BH3-only proteins: orchestrators of apoptosis. Biochim Biophys Acta-Mol Cell Res 1813:508–520
Shamas-Din A, Bindner S, Chi X, Leber B, Andrews DW, Fradin C (2015) Distinct lipid effects on tBid and Bim activation of membrane permeabilization by pro-apoptotic Bax. Biochem J 467:495–505
Shivakumar S, Kurylowicz M, Hirmiz N, Manan Y, Friaa O, Shamas-Din A, Masoudian P, Leber B, Andrews DW, Fradin C (2014) The proapoptotic protein tBid forms both superficially bound and membrane-inserted oligomers. Biophys J 106:2085–2095
Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103:645–654
Tait SW, Green DR (2010) Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11:621–632
Terrones O, Antonsson B, Yamaguchi H, Wang H-G, Liu J, Lee RM, Herrmann A, Basañez G (2004) Lipidic pore formation by the concerted action of proapoptotic BAX and tBID. J Biol Chem 279:30081–30091
Torrecillas A, Martínez-Senac MM, Ausili A, Corbalán-García S, Gómez-Fernández JC (2007) Interaction of the C-terminal domain of Bcl-2 family proteins with model membranes. Biochim Biophys Acta-Biomembr 1768:2931–2939
Tyurin VA, Tyurina YY, Kochanek PM, Hamilton R, DeKosky ST, Greenberger JS, Bayir H, Kagan VE (2008) Chapter nineteen oxidative lipidomics of programmed cell death. Methods Enzymol 442:375–393
Uren RT, Dewson G, Chen L, Coyne SC, Huang DC, Adams JM, Kluck RM (2007) Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak. J Cell Biol 177:277–287
Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060–2071
Westphal D, Dewson G, Czabotar PE, Kluck RM (2011) Molecular biology of Bax and Bak activation and action. Biochim Biophys Acta-Mol Cell Res 1813:521–531
Westphal D, Kluck R, Dewson G (2014) Building blocks of the apoptotic pore: how Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ 21:196–205
Wong RS (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res 30:87
Yethon JA, Epand RF, Leber B, Epand RM, Andrews DW (2003) Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J Biol Chem 278:48935–48941
Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59
Zaltsman Y, Shachnai L, Yivgi-Ohana N, Schwarz M, Maryanovich M, Houtkooper RH, Vaz FM, De Leonardis F, Fiermonte G, Palmieri F (2010) MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat Cell Biol 12:553–562
Zhang Z, Subramaniam S, Kale J, Liao C, Huang B, Brahmbhatt H, Condon SG, Lapolla SM, Hays FA, Ding J (2015) BH3-in-groove dimerization initiates and helix 9 dimerization expands Bax pore assembly in membranes. EMBO J 35:208–236
Zong W-X, Lindsten T, Ross AJ, MacGregor GR, Thompson CB (2001) BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 15:1481–1486
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Siti Haji Suhaili declares that she has no conflicts of interest. Hamed Karimian declares that he has no conflicts of interest. Matthew Stellato declares that he has no conflicts of interest. Tzong-Hsien Lee declares that he has no conflicts of interest. Marie-Isabel Aguilar declares that she has no conflicts of interest.
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Suhaili, S.H., Karimian, H., Stellato, M. et al. Mitochondrial outer membrane permeabilization: a focus on the role of mitochondrial membrane structural organization. Biophys Rev 9, 443–457 (2017). https://doi.org/10.1007/s12551-017-0308-0
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DOI: https://doi.org/10.1007/s12551-017-0308-0