SAM50, a side door to the mitochondria: The case of cytotoxic proteases

Bachmann, 1994, Induction of protective cytotoxic T cells with viral proteins, Eur. J. Immunol., 24, 2228, 10.1002/eji.1830240944 Kagi, 1996, Different roles for cytotoxic T cells in the control of infections with cytopathic versus noncytopathic viruses, Curr. Opin. Immunol., 8, 472, 10.1016/S0952-7915(96)80033-1 Kagi, 1994, CD8+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity, Eur. J. Immunol., 24, 3068, 10.1002/eji.1830241223 van den Broek, 1996, Decreased tumor surveillance in perforin-deficient mice, J. Exp. Med., 184, 1781, 10.1084/jem.184.5.1781 Senovilla, 2012, An immunosurveillance mechanism controls cancer cell ploidy, Science, 337, 1678, 10.1126/science.1224922 Shankaran, 2001, IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity, Nature, 410, 1107, 10.1038/35074122 Law, 2010, The structural basis for membrane binding and pore formation by lymphocyte perforin, Nature, 468, 447, 10.1038/nature09518 Thiery, 2011, Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells, Nat. Immunol., 12, 770, 10.1038/ni.2050 Thiery, 2010, Perforin activates clathrin- and dynamin-dependent endocytosis, which is required for plasma membrane repair and delivery of granzyme B for granzyme-mediated apoptosis, Blood, 115, 1582, 10.1182/blood-2009-10-246116 Berke, 1991, T-cell-mediated cytotoxicity, Curr. Opin. Immunol., 3, 320, 10.1016/0952-7915(91)90031-U Trenn, 1987, Exocytosis of cytolytic granules may not be required for target cell lysis by cytotoxic T-lymphocytes, Nature, 330, 72, 10.1038/330072a0 Ostergaard, 1987, Cytotoxic T lymphocyte mediated lysis without release of serine esterase, Nature, 330, 71, 10.1038/330071a0 Rouvier, 1993, Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity, J. Exp. Med., 177, 195, 10.1084/jem.177.1.195 Kagi, 1994, Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice, Nature, 369, 31, 10.1038/369031a0 Kagi, 1994, Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity, Science, 265, 528, 10.1126/science.7518614 Peters, 1991, Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes, J. Exp. Med., 173, 1099, 10.1084/jem.173.5.1099 Russell, 2002, Lymphocyte-mediated cytotoxicity, Annu. Rev. Immunol., 20, 323, 10.1146/annurev.immunol.20.100201.131730 Bossi, 1999, Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells, Nat. Med., 5, 90, 10.1038/4779 Lee, 2018, Fas Ligand localizes to intraluminal vesicles within NK cell cytolytic granules and is enriched at the immune synapse, Immun. Inflamm. Dis., 6, 312, 10.1002/iid3.219 Chowdhury, 2008, Death by a thousand cuts: granzyme pathways of programmed cell death, Annu. Rev. Immunol., 26, 389, 10.1146/annurev.immunol.26.021607.090404 Sattar, 2003, Bioinformatics of granzymes: sequence comparison and structural studies on granzyme family by homology modeling, Biochem. Biophys. Res. Commun., 308, 726, 10.1016/S0006-291X(03)01458-X Masson, 1987, A family of serine esterases in lytic granules of cytolytic T lymphocytes, Cell, 49, 679, 10.1016/0092-8674(87)90544-7 Beresford, 1999, Granzyme A loading induces rapid cytolysis and a novel form of DNA damage independently of caspase activation, Immunity, 10, 585, 10.1016/S1074-7613(00)80058-8 Lieberman, 2010, Granzyme A activates another way to die, Immunol. Rev., 235, 93, 10.1111/j.0105-2896.2010.00902.x Martinvalet, 2005, Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis, Immunity, 22, 355, 10.1016/j.immuni.2005.02.004 Zhang, 2001, Granzymes A and B directly cleave lamins and disrupt the nuclear lamina during granule-mediated cytolysis, Proc. Natl. Acad. Sci. U.S.A., 98, 5746, 10.1073/pnas.101329598 Zhu, 2006, Granzyme A, which causes single-stranded DNA damage, targets the double-strand break repair protein Ku70, EMBO Rep., 7, 431, 10.1038/sj.embor.7400622 Odake, 1991, Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins, Biochemistry, 30, 2217, 10.1021/bi00222a027 Sutton, 2003, Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors, Immunity, 18, 319, 10.1016/S1074-7613(03)00050-5 Goping, 2003, Granzyme B-induced apoptosis requires both direct caspase activation and relief of caspase inhibition, Immunity, 18, 355, 10.1016/S1074-7613(03)00032-3 Kaiserman, 2006, The major human and mouse granzymes are structurally and functionally divergent, J. Cell Biol., 175, 619, 10.1083/jcb.200606073 Sutton, 1997, Bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes, J. Immunol., 158, 5783, 10.4049/jimmunol.158.12.5783 Andrade, 1998, Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis, Immunity, 8, 451, 10.1016/S1074-7613(00)80550-6 Cullen, 2007, Human and murine granzyme B exhibit divergent substrate preferences, J. Cell Biol., 176, 435, 10.1083/jcb.200612025 Sutton, 2000, Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation, J. Exp. Med., 192, 1403, 10.1084/jem.192.10.1403 Waterhouse, 2005, A central role for Bid in granzyme B-induced apoptosis, J. Biol. Chem., 280, 4476, 10.1074/jbc.M410985200 Alimonti, 2001, Granzyme B induces BID-mediated cytochrome c release and mitochondrial permeability transition, J. Biol. Chem., 276, 6974, 10.1074/jbc.M008444200 Casciola-Rosen, 2007, Mouse and human granzyme B have distinct tetrapeptide specificities and abilities to recruit the bid pathway, J. Biol. Chem., 282, 4545, 10.1074/jbc.M606564200 Han, 2010, Deregulation of mitochondrial membrane potential by mitochondrial insertion of granzyme B and direct Hax-1 cleavage, J. Biol. Chem., 285, 22461, 10.1074/jbc.M109.086587 Kroemer, 2007, Mitochondrial membrane permeabilization in cell death, Physiol. Rev., 87, 99, 10.1152/physrev.00013.2006 MacDonald, 1999, Mitochondria-dependent and -independent regulation of Granzyme B-induced apoptosis, J. Exp. Med., 189, 131, 10.1084/jem.189.1.131 Parrish, 2001, Mitochondrial endonuclease G is important for apoptosis in C. Elegans, Nature, 412, 90, 10.1038/35083608 Susin, 1999, Molecular characterization of mitochondrial apoptosis-inducing factor, Nature, 397, 441, 10.1038/17135 Heibein, 1999, Granzyme B-induced loss of mitochondrial inner membrane potential (Delta psi m) and cytochrome c release are caspase independent, J. Immunol., 163, 4683, 10.4049/jimmunol.163.9.4683 Thomas, 2001, Granzyme B can cause mitochondrial depolarization and cell death in the absence of BID, BAX, and BAK, Proc. Natl. Acad. Sci. U.S.A., 98, 14985, 10.1073/pnas.261581498 Chiusolo, 2017, Granzyme B enters the mitochondria in a Sam50-, Tim22- and mtHsp70-dependent manner to induce apoptosis, Cell Death Differ., 24, 747, 10.1038/cdd.2017.3 Jacquemin, 2015, Granzyme B-induced mitochondrial ROS are required for apoptosis, Cell Death Differ., 22, 862, 10.1038/cdd.2014.180 Martinvalet, 2008, Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death, Cell, 133, 681, 10.1016/j.cell.2008.03.032 Ricci, 2004, Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain, Cell, 117, 773, 10.1016/j.cell.2004.05.008 Trapani, 2002, Functional significance of the perforin/granzyme cell death pathway, Nat. Rev. Immunol., 2, 735, 10.1038/nri911 Trapani, 2012, Granzymes, cytotoxic granules and cell death: the early work of Dr, Jurg Tschopp, Cell death and differentiation, 19, 21, 10.1038/cdd.2011.156 Lang, 1997, An ancestral mitochondrial DNA resembling a eubacterial genome in miniature, Nature, 387, 493, 10.1038/387493a0 Vendramin, 2017, Non-coding RNAs: the dark side of nuclear-mitochondrial communication, EMBO J., 36, 1123, 10.15252/embj.201695546 Martijn, 2018, Deep mitochondrial origin outside the sampled alphaproteobacteria, Nature, 557, 101, 10.1038/s41586-018-0059-5 Mannella, 2013, The connection between inner membrane topology and mitochondrial function, J. Mol. Cell. Cardiol., 62, 51, 10.1016/j.yjmcc.2013.05.001 Mannella, 1994, The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope, Microsc. Res. Tech., 27, 278, 10.1002/jemt.1070270403 van der Laan, 2012, Role of MINOS in mitochondrial membrane architecture and biogenesis, Trends Cell Biol., 22, 185, 10.1016/j.tcb.2012.01.004 Kozjak-Pavlovic, 2017, The MICOS complex of human mitochondria, Cell Tissue Res., 367, 83, 10.1007/s00441-016-2433-7 Li, 2016, Mic60/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization, Cell Death Differ., 23, 380, 10.1038/cdd.2015.102 Ott, 2015, Detailed analysis of the human mitochondrial contact site complex indicate a hierarchy of subunits, PLoS One, 10, 10.1371/journal.pone.0120213 Attardi, 1988, Biogenesis of mitochondria, Annu. Rev. Cell Biol., 4, 289, 10.1146/annurev.cb.04.110188.001445 McBride, 2006, Mitochondria: more than just a powerhouse, Curr. Biol., 16, R551, 10.1016/j.cub.2006.06.054 Saraste, 1999, Oxidative phosphorylation at the fin de siecle, Science, 283, 1488, 10.1126/science.283.5407.1488 Mitchell, 1961, Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism, Nature, 191, 144, 10.1038/191144a0 Murphy, 2009, How mitochondria produce reactive oxygen species, Biochem. J., 417, 1, 10.1042/BJ20081386 Baughman, 2011, Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter, Nature, 476, 341, 10.1038/nature10234 Bernardi, 1999, Mitochondria and cell death. Mechanistic aspects and methodological issues, Eur. J. Biochem., 264, 687, 10.1046/j.1432-1327.1999.00725.x Hajnoczky, 2006, Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis, Cell Calcium, 40, 553, 10.1016/j.ceca.2006.08.016 Bernardi, 2015, The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology, Physiol. Rev., 95, 1111, 10.1152/physrev.00001.2015 Rasola, 2011, Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis, Cell Calcium, 50, 222, 10.1016/j.ceca.2011.04.007 Bernardi, 2018, Why F-ATP synthase remains a strong candidate as the mitochondrial permeability transition pore, Front. Physiol., 9, 1543, 10.3389/fphys.2018.01543 De Stefani, 2011, A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter, Nature, 476, 336, 10.1038/nature10230 Breitenbach, 2013, Mitochondria in ageing: there is metabolism beyond the ROS, FEMS Yeast Res. Chan, 2006, Mitochondria: dynamic organelles in disease, aging, and development, Cell, 125, 1241, 10.1016/j.cell.2006.06.010 Green, 2004, The pathophysiology of mitochondrial cell death, Science, 305, 626, 10.1126/science.1099320 Tait, 2010, Mitochondria and cell death: outer membrane permeabilization and beyond, Nature reviews, Molecular cell biology, 11, 621 Kasahara, 2013, Mitochondrial fusion directs cardiomyocyte differentiation via calcineurin and Notch signaling, Science, 342, 734, 10.1126/science.1241359 Kasahara, 2014, Mitochondria: from cell death executioners to regulators of cell differentiation, Trends Cell Biol., 24, 761, 10.1016/j.tcb.2014.08.005 Rizzuto, 2000, Mitochondria as all-round players of the calcium game, J. Physiol. (Paris), 529, 37 Morgenstern, 2017, Definition of a high-confidence mitochondrial proteome at quantitative scale, Cell Rep., 19, 2836, 10.1016/j.celrep.2017.06.014 Calvo, 2016, MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins, Nucleic Acids Res., 44, D1251, 10.1093/nar/gkv1003 Pfanner, 2019, Mitochondrial proteins: from biogenesis to functional networks, Nature reviews, Molecular cell biology, 20, 267 Westermann, 2010, Mitochondrial fusion and fission in cell life and death, Nature reviews, Molecular cell biology, 11, 872 Chan, 2012, Fusion and fission: interlinked processes critical for mitochondrial health, Annu. Rev. Genet., 46, 265, 10.1146/annurev-genet-110410-132529 Cereghetti, 2010, Inhibition of Drp1-dependent mitochondrial fragmentation and apoptosis by a polypeptide antagonist of calcineurin, Cell Death Differ., 17, 1785, 10.1038/cdd.2010.61 Cereghetti, 2008, Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria, Proc. Natl. Acad. Sci. U.S.A., 105, 15803, 10.1073/pnas.0808249105 Dimmer, 2006, (De)constructing mitochondria: what for?, Physiology Bethesda (Bethesda), 21, 233 Frezza, 2006, OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion, Cell, 126, 177, 10.1016/j.cell.2006.06.025 Gomes, 2011, During autophagy mitochondria elongate, are spared from degradation and sustain cell viability, Nat. Cell Biol., 13, 589, 10.1038/ncb2220 Scorrano, 2005, Proteins that fuse and fragment mitochondria in apoptosis: con-fissing a deadly con-fusion?, J. Bioenerg. Biomembr., 37, 165, 10.1007/s10863-005-6572-x Gandre-Babbe, 2008, The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells, Mol. Biol. Cell, 19, 2402, 10.1091/mbc.e07-12-1287 Otera, 2010, Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells, J. Cell Biol., 191, 1141, 10.1083/jcb.201007152 Palmer, 2011, MiD49 and MiD51, new components of the mitochondrial fission machinery, EMBO Rep., 12, 565, 10.1038/embor.2011.54 Zhao, 2011, Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission, EMBO J., 30, 2762, 10.1038/emboj.2011.198 Rehling, 2004, Mitochondrial import and the twin-pore translocase, Nature reviews, Molecular cell biology, 5, 519 Hill, 1998, Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins [see comment], Nature, 395, 516, 10.1038/26780 Araiso, 2019, Structure of the mitochondrial import gate reveals distinct preprotein paths, Nature, 575, 395, 10.1038/s41586-019-1680-7 Tucker, 2019, Cryo-EM structure of the mitochondrial protein-import channel TOM complex at near-atomic resolution, Nat. Struct. Mol. Biol., 26, 1158, 10.1038/s41594-019-0339-2 Bauer, 1996, Role of Tim23 as voltage sensor and presequence receptor in protein import into mitochondria, Cell, 87, 33, 10.1016/S0092-8674(00)81320-3 Malhotra, 2013, Structural changes in the mitochondrial Tim23 channel are coupled to the proton-motive force, Nat. Struct. Mol. Biol., 20, 965, 10.1038/nsmb.2613 D’Silva, 2004, Regulated interactions of mtHsp70 with Tim44 at the translocon in the mitochondrial inner membrane, Nat. Struct. Mol. Biol., 11, 1084, 10.1038/nsmb846 Schneider, 1994, Mitochondrial Hsp70/MIM44 complex facilitates protein import, Nature, 371, 768, 10.1038/371768a0 Hawlitschek, 1988, Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein, Cell, 53, 795, 10.1016/0092-8674(88)90096-7 Popov-Celeketic, 2008, Mim1 functions in an oligomeric form to facilitate the integration of Tom20 into the mitochondrial outer membrane, J. Mol. Biol., 376, 671, 10.1016/j.jmb.2007.12.006 Chacinska, 2004, Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins, EMBO J., 23, 3735, 10.1038/sj.emboj.7600389 Gebert, 2011, Dual function of Sdh3 in the respiratory chain and TIM22 protein translocase of the mitochondrial inner membrane, Mol. Cell, 44, 811, 10.1016/j.molcel.2011.09.025 Kerscher, 2000, Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane, Mol. Biol. Cell, 11, 103, 10.1091/mbc.11.1.103 Kovermann, 2002, Tim22, the essential core of the mitochondrial protein insertion complex, forms a voltage-activated and signal-gated channel, Mol. Cell, 9, 363, 10.1016/S1097-2765(02)00446-X Klein, 2012, Characterization of the insertase for beta-barrel proteins of the outer mitochondrial membrane, J. Cell Biol., 199, 599, 10.1083/jcb.201207161 Paschen, 2003, Evolutionary conservation of biogenesis of beta-barrel membrane proteins, Nature, 426, 862, 10.1038/nature02208 Hohr, 2018, Membrane protein insertion through a mitochondrial beta-barrel gate, Science, 359, 10.1126/science.aah6834 Nargund, 2012, Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation, Science, 337, 587, 10.1126/science.1223560 Wang, 2015, A cytosolic network suppressing mitochondria-mediated proteostatic stress and cell death, Nature, 524, 481, 10.1038/nature14859 Wiedemann, 2017, Mitochondrial machineries for protein import and assembly, Annu. Rev. Biochem., 86, 685, 10.1146/annurev-biochem-060815-014352 Brough, 2005, Agonist-induced regulation of mitochondrial and endoplasmic reticulum motility, Biochem. J., 392, 291, 10.1042/BJ20050738 Yi, 2004, Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit, J. Cell Biol., 167, 661, 10.1083/jcb.200406038 Friedman, 2011, ER tubules mark sites of mitochondrial division, Science, 334, 358, 10.1126/science.1207385 Rizzuto, 1993, Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria, Science, 262, 744, 10.1126/science.8235595 Rizzuto, 1998, Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses, Science, 280, 1763, 10.1126/science.280.5370.1763 Rowland, 2012, Endoplasmic reticulum-mitochondria contacts: function of the junction, Nature reviews, Molecular cell biology, 13, 607 Korobova, 2013, An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2, Science, 339, 464, 10.1126/science.1228360 Hayashi, 2009, MAM: more than just a housekeeper, Trends Cell Biol., 19, 81, 10.1016/j.tcb.2008.12.002 Hamasaki, 2013, Autophagosomes form at ER-mitochondria contact sites, Nature, 495, 389, 10.1038/nature11910 Kornmann, 2009, An ER-mitochondria tethering complex revealed by a synthetic biology screen, Science, 325, 477, 10.1126/science.1175088 Phillips, 2016, Structure and function of ER membrane contact sites with other organelles, Nature reviews, Molecular cell biology, 17, 69 Korobova, 2014, A role for myosin II in mammalian mitochondrial fission, Curr. Biol., 24, 409, 10.1016/j.cub.2013.12.032 Mears, 2011, Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission, Nat. Struct. Mol. Biol., 18, 20, 10.1038/nsmb.1949 Ingerman, 2005, Dnm1 forms spirals that are structurally tailored to fit mitochondria, J. Cell Biol., 170, 1021, 10.1083/jcb.200506078 Yoon, 2001, Mammalian dynamin-like protein DLP1 tubulates membranes, Mol. Biol. Cell, 12, 2894, 10.1091/mbc.12.9.2894 Brooks, 2007, Bak regulates mitochondrial morphology and pathology during apoptosis by interacting with mitofusins, Proc. Natl. Acad. Sci. U.S.A., 104, 11649, 10.1073/pnas.0703976104 Karbowski, 2004, Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis, J. Cell Biol., 164, 493, 10.1083/jcb.200309082 Karbowski, 2002, Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis, J. Cell Biol., 159, 931, 10.1083/jcb.200209124 Wasiak, 2007, Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death, J. Cell Biol., 177, 439, 10.1083/jcb.200610042 Qi, 2011, Aberrant mitochondrial fission in neurons induced by protein kinase C{delta} under oxidative stress conditions in vivo, Mol. Biol. Cell, 22, 256, 10.1091/mbc.e10-06-0551 Griparic, 2007, Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage, J. Cell Biol., 178, 757, 10.1083/jcb.200704112 Ishihara, 2006, Regulation of mitochondrial morphology through proteolytic cleavage of OPA1, EMBO J., 25, 2966, 10.1038/sj.emboj.7601184 Martinvalet, 2015, ROS signaling during granzyme B-mediated apoptosis, Mol. Cell. Oncol., 2 Beresford, 2001, Granzyme A activates an endoplasmic reticulum-associated caspase-independent nuclease to induce single-stranded DNA nicks, J. Biol. Chem., 276, 43285, 10.1074/jbc.M108137200 Chowdhury, 2006, The exonuclease TREX1 is in the SET complex and acts in concert with NM23-H1 to degrade DNA during granzyme A-mediated cell death, Mol. Cell, 23, 133, 10.1016/j.molcel.2006.06.005 Fan, 2003, Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor, Cell, 112, 659, 10.1016/S0092-8674(03)00150-8 Fan, 2002, HMG2 interacts with the nucleosome assembly protein SET and is a target of the cytotoxic T-lymphocyte protease granzyme A, Mol. Cell. Biol., 22, 2810, 10.1128/MCB.22.8.2810-2820.2002 Fan, 2003, Cleaving the oxidative repair protein Ape1 enhances cell death mediated by granzyme A, Nat. Immunol., 4, 145, 10.1038/ni885 Sazanov, 2006, Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus, Science, 311, 1430, 10.1126/science.1123809 Walch, 2014, Cytotoxic cells kill intracellular Bacteria through granulysin-mediated delivery of granzymes, Cell, 157, 1309, 10.1016/j.cell.2014.03.062 Dotiwala, 2017, Granzyme B Disrupts Central Metabolism and Protein Synthesis in Bacteria to Promote an Immune Cell Death Program, Cell, 171, 1125, 10.1016/j.cell.2017.10.004 Wei, 2001, Proapoptotic B.A.X. and BAK: a requisite gateway to mitochondrial dysfunction and death, Science, 292, 727, 10.1126/science.1059108 Petrosillo, 2003, Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria, FASEB J., 17, 2202, 10.1096/fj.03-0012com Petrosillo, 2004, Ca2+-induced reactive oxygen species production promotes cytochrome c release from rat liver mitochondria via mitochondrial permeability transition (MPT)-dependent and MPT-independent mechanisms: role of cardiolipin, J. Biol. Chem., 279, 53103, 10.1074/jbc.M407500200 Chacinska, 2009, Importing mitochondrial proteins: machineries and mechanisms, Cell, 138, 628, 10.1016/j.cell.2009.08.005 Rehling, 2003, Protein insertion into the mitochondrial inner membrane by a twin-pore translocase, Science, 299, 1747, 10.1126/science.1080945 Gentle, 2004, The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria, J. Cell Biol., 164, 19, 10.1083/jcb.200310092 Moslavac, 2005, Conserved pore-forming regions in polypeptide-transporting proteins, FEBS J., 272, 1367, 10.1111/j.1742-4658.2005.04569.x Estebanez-Perpina, 2000, Crystal structure of the caspase activator human granzyme B, a proteinase highly specific for an Asp-P1 residue, Biol. Chem., 381, 1203, 10.1515/BC.2000.148 Andres, 2010, The TOC complex: preprotein gateway to the chloroplast, Biochim. Biophys. Acta, 1803, 715, 10.1016/j.bbamcr.2010.03.004 Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res., 46, W296, 10.1093/nar/gky427 Bienert, 2017, The SWISS-MODEL Repository-new features and functionality, Nucleic Acids Res., 45, D313, 10.1093/nar/gkw1132 Guex, 2009, Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective, Electrophoresis, 30, S162, 10.1002/elps.200900140 Benkert, 2011, Toward the estimation of the absolute quality of individual protein structure models, Bioinformatics, 27, 343, 10.1093/bioinformatics/btq662 Bertoni, 2017, Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology, Sci. Rep., 7, 10480, 10.1038/s41598-017-09654-8 Jans, 2013, STED super-resolution microscopy reveals an array of MINOS clusters along human mitochondria, Proc. Natl. Acad. Sci. U.S.A., 110, 8936, 10.1073/pnas.1301820110 Xie, 2007, The mitochondrial inner membrane protein mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11, FEBS Lett., 581, 3545, 10.1016/j.febslet.2007.06.052