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1.B.8 The Mitochondrial and Plastid Porin (MPP) Family

Porins of the MPP family are found in eukaryotic organelles. The organelles include mitochondria of many eukaryotes as well as chloroplasts and plastids of plants. The best characterized members of the MPP family are the voltage-dependent anion-selective channel (VDAC) porins in the mitochondrial outer membrane. These porins have an estimated channel diameter of 2.5-3 nm. Topological models have been proposed in which VDAC consists of an N-terminal, globular α-helix and (1) 12 or 13 β-strands, (2) 16 β-strands or (3) 19 β-strands (now favored; see below) (Casadio et al., 2002). VDAC also appears to be present in plasma membranes (De Pinto et al., 2010). Prostacyclin receptor-mediated ATP release from ethrocytes requires VDAC (Sridharan et al., 2011).  Phylogenetic analyses of eukaryotic VDAC proteins from diverse organisms have been reported (Wojtkowska et al. 2012). Over-oxidation of cysteines and succinylation of cysteines in VDACs has been noticed (Saletti et al. 2018).

A murine VDAC, VDAC-1, exhibits more than one topological type due to the use of alternative first exons. Thus, two different porins, differing only with respect to their N-termini, have been identified. One porin isoform (plasmalemmal VDAC-1) has a hydrophobic leader peptide that targets the protein through the golgi apparatus to the plasma membrane; the other isoform (mitochondrial VDAC-1) is translocated to the outer mitochondrial membrane because it lacks the N-terminal hydrophobic leader. The former is believed to account for the plasma membrane Maxi (large conductance) Cl- channel (Bahamonde et al., 2003). 

VDACs play a role in forming the mitochondrial permeability transition pore (PTP) which is important for Ca2+ homeostasis and programmed cell death. PTP is triggered by Ca2+ influx into mitochondria, and VDAC is permeable to Ca2+. It is also regulated by various compounds such as glutamate, NADH and nucleotides. VDAC has two nucleotide binding sites (Yehezkel et al., 2006). In VDAC1 the two cysteine residues seem not to be required for apoptosis or VDAC1 oligomerization (Aram et al., 2010).  Ions interact intimately with the inner walls of the channel and are selected by their 3-dimensional structure, not merely by their size and charge (Colombini 2016).  The N-terminus acts not as a gate on a stable barrel, but rather stabilizes the barrel, preventing its shift into a partially collapsed, low-conductance, closed state (Shuvo et al. 2016).

Mutations in superoxide dismutase (SOD1) cause amyotrophic lateral sclerosis (ALS), a neurodegenerative disease characterized by loss of motor neurons. Misfolded mutant SOD1 binds directly to VDAC1. Direct binding of mutant SOD1 to VDAC1 inhibits conductance of channels when reconstituted in a lipid bilayer (Israelson et al., 2010). 

VDAC-protein interactions for each mammalian isoform (VDAC1, 2 and 3)  showed that VDAC1 is mainly involved in the maintenance of cellular homeostasis and in pro-apoptotic processes, whereas VDAC2 displays an anti-apoptotic role, while VDAC3 may contribute to mitochondrial protein quality control and act as a marker of oxidative status (Caterino et al. 2017). In pathological conditions, namely neurodegenerative and cardiovascular diseases, both VDAC1 and VDAC2 establish abnormal interactions aimed to counteract the mitochondrial dysfunction which contributes to end-organ damage.

Persistent opening of PTP creates a bioenergetic crisis with collapse of the membrane potential, ATP depletion, Ca2+ deregulation, and release of proteins such as cytochrome c into the cytoplasm. These events promote cell death. The PTP traverses the inner and outer membranes and involves the ATP/ADP exchanger in the inner membrane and VDAC in the other membrane (Cesura et al., 2003). Another postulate suggests that a calcium-triggered conformational change of the mitochondrial phosphate carrier (PiC), facilitated by cyclophilin-D (CyP-D), induces pore opening. This is enhanced by an association of the PiC with the 'c' conformation of the ANT. Agents that modulate pore opening may act on either or both the PiC and the ANT (Leung and Halestrap, 2008).

The selective anti-tumour agent erastin causes the appearance of oxidative species and subsequent death through an oxidative, non-apoptotic mechanism. RNA-interference-mediated knockdown of VDAC2 or VDAC3 caused resistance to erastin. Using purified mitochondria expressing a single VDAC isoform, erastin alters the permeability of the outer mitochondrial membrane by binding directly to VDAC2. Thus, ligands to VDAC proteins can induce non-apoptotic cell death selectively in some tumour cells harbouring activating mutations in the RAS-RAF-MEK pathway (Yagoda et al., 2007).

It forms a 19-stranded beta barrel with the first and last strand parallel. The hydrophobic outside perimeter of the barrel is covered by detergent molecules in a beltlike fashion (Hiller et al., 2010). In the presence of cholesterol, recombinant VDAC-1 can form voltage-gated channels in phospholipid bilayers similar to those of the native protein. The NMR measurements revealed the binding sites of VDAC-1 for the Bcl-2 protein, Bcl-x(L), for reduced beta-nicotinamide adenine dinucleotide, and for cholesterol. Bcl-x(L) interacts with the VDAC barrel laterally at strands 17 and 18 (Hiller et al., 2008). The position of the voltage-sensing N-terminal segment is oriented against the interior wall, causing a partial narrowing at the center of the pore. This segment is ideally positioned to regulate the conductance of ions and metabolites passing through the VDAC pore (Ujwal et al., 2008). 

Mitochondria import 90-99% of their proteins from the cytosol. Three protein families including Sam50, VDAC and Tom40 together with Mdm10 compose the set of integral beta-barrel proteins embedded in the mitochondrial outer membrane in S. cerevisiae (MOM) (Zeth 2010). The 16-stranded Sam50 protein forms part of the sorting and assembly machinery (SAM) and shows a clear evolutionary relationship to members of the bacterial Omp85 family (1.B.33). VDAC and Tom40 both adopt the same fold with 19 probable TMSs. Tom40 is in the TOM complex (3.A.8). Models of Tom40 and Sam50 have been developed using X-ray structures of related proteins. These models have been analyzed with respect to properties such as conservation and charge distribution yielding features related to their individual functions (Zeth 2010). 

The gene for VDAC1 in humans is over-expressed in many cancer types, and silencing of VDAC1 expression inhibits tumor development. Along with regulating cellular energy production and metabolism, VDAC1 is involved in the process of apoptosis by mediating the release of apoptotic proteins and interacting with anti-apoptotic proteins. The engagement of VDAC1 in the release of apoptotic proteins located in the inter-membranal space involves VDAC1 oligomerization that mediates the release of cytochrome c and AIF to the cytosol, subsequently leading to apoptotic cell death (Shoshan-Barmatz et al. 2015).

Under cellular stress, human VDACs hetero-oligomerize and coaggregate with proteins that can form amyloidogenic and neurodegenerative deposits, implicating a role for VDACs in proteotoxicity. Gupta and Mahalakshmi 2019 mapped aggregation-prone regions of human VDACs, using isoform 3 as the model VDAC, and showed that the region comprising strands beta7-beta9 is aggregation prone. An alpha1-beta7-beta9 interaction (involving the hVDAC3 N-terminal alpha1 helix) can lower protein aggregation, whereas perturbations of this interaction promote VDAC aggregation. hVDAC3 aggregation proceeds via a partially unfolded structure.

The generalized transport reaction catalyzed by VDACs is:

(Anionic) metabolites (out) ↔ anionic metabolites (intermembrane space)

References associated with 1.B.8 family:

Aiello R., A. Messina, B. Schiffler, R. Benz, G. Tasco, R. Casadio, V. De Pinto. (2004). Functional characterization of a second porin isoform in Drosophila melanogaster. DmPorin2 forms voltage-independent cation-selective pores. J Biol Chem. 279:25364-25373. 15054101
Aram L., Geula S., Arbel N. and Shoshan-Barmatz V. (2010). VDAC1 cysteine residues: topology and function in channel activity and apoptosis. Biochem J. 427(3):445-54. 20192921
Austin, C.J., J. Kahlert, M. Kassiou, and L.M. Rendina. (2013). The translocator protein (TSPO): a novel target for cancer chemotherapy. Int J Biochem. Cell Biol. 45: 1212-1216. 23518318
Bahamonde, M.I., J.M. Fernández-Fernández, F.X. Guix, E. Vázquez, and M.A. Valverde. (2003). Plasma membrane voltage-dependent anion channel mediates antiestrogen-activated Maxi Cl- currents in C1300 neuroblastoma cells. J. Biol. Chem. 278: 33284-33289. 12794078
Bayrhuber, M., T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, and K. Zeth. (2008). Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 105: 15370-15375. 18832158
Bergdoll, L.A., M.T. Lerch, J.W. Patrick, K. Belardo, C. Altenbach, P. Bisignano, A. Laganowsky, M. Grabe, W.L. Hubbell, and J. Abramson. (2018). Protonation state of glutamate 73 regulates the formation of a specific dimeric association of mVDAC1. Proc. Natl. Acad. Sci. USA 115: E172-E179. 29279396
Blachly-Dyson, E., S. Peng, M. Colombini, and M. Forte. (1990). Selectivity changes in the site-directed mutants of the VDAC ion channel: structural implications. Science 247: 1233-1236. 1690454
Buettner, R., G. Papoutsoglou, E. Scemes, D.C. Spray, and R. Dermietzel. (2000). Evidence for secretory pathway localization of a voltage-dependent anion channel isoform. Proc. Natl. Acad. Sci. USA 97: 3201-3206. 10716730
Casadio, R., I. Jacoboni, A. Messina, and V. De Pinto. (2002). A 3D model of the voltage-dependent anion channel (VDAC). FEBS Lett. 520: 1-7. 12044860
Caterino, M., M. Ruoppolo, A. Mandola, M. Costanzo, S. Orrù, and E. Imperlini. (2017). Protein-protein interaction networks as a new perspective to evaluate distinct functional roles of voltage-dependent anion channel isoforms. Mol Biosyst 13: 2466-2476. 29028058
Cesura, A.M., E. Pinard, R. Schubenel, V. Goetschy, A. Friedlein, H. Langen, P. Polcic, M.A. Forte, P. Bernardi, and J.A. Kemp. (2003). The voltage-dependent anion channel is the target for a new class of inhibitors of the mitochondrial permeability transition pore. J. Biol. Chem. 278: 49812-49818. 12952973
Checchetto, V., S. Reina, A. Magrì, I. Szabo, and V. De Pinto. (2014). Recombinant Human Voltage Dependent Anion Selective Channel Isoform 3 (hVDAC3) Forms Pores with a Very Small Conductance. Cell Physiol Biochem 34: 842-853. 25171321
Colombini, M. (2016). The VDAC channel: Molecular basis for selectivity. Biochim. Biophys. Acta. [Epub: Ahead of Print] 26826035
Craigen, W.J. and B.H. Graham. (2008). Genetic strategies for dissecting mammalian and Drosophila voltage-dependent anion channel functions. J. Bioenerg. Biomembr. 40: 207-212. 18622693
De Pinto, V., A. Messina, D.J. Lane, and A. Lawen. (2010). Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Lett. 584: 1793-1799. 20184885
De Pinto, V., R. Benz, C. Caggese, and F. Palmieri. (1989). Characterization of the mitochondrial porin from Drosophila melanogaster. Biochim. Biophys. Acta. 987: 1-7. 2480813
Fischer, K., A. Weber, S. Brink, B. Arbinger, D. Schünemann, S. Borchert, H.W. Heldt, B. Popp, R. Benz, T.A. Link, C. Eckerskorn, and U.-I. Flügge. (1994). Porins from plants: molecular cloning and functional characterization of two new members of the porin family. J. Biol. Chem. 269: 25754-25760. 7523392
Flinner, N., L. Ellenrieder, S.B. Stiller, T. Becker, E. Schleiff, and O. Mirus. (2013). Mdm10 is an ancient eukaryotic porin co-occurring with the ERMES complex. Biochim. Biophys. Acta. 1833: 3314-3325. 24135058
Godbole, A., R. Mitra, A.K. Dubey, P.S. Reddy, and M.K. Mathew. (2011). Bacterial expression, purification and characterization of a rice voltage-dependent, anion-selective channel isoform, OsVDAC4. J. Membr. Biol. 244: 67-80. 22057934
Graham, B.H., Z. Li, E.P. Alesii, P. Versteken, C. Lee, J. Wang, and W.J. Craigen. (2010). Neurologic dysfunction and male infertility in Drosophila porin mutants: a new model for mitochondrial dysfunction and disease. J. Biol. Chem. 285: 11143-11153. 20110367
Guardiani, C., A. Magrì, A. Karachitos, M.C. Di Rosa, S. Reina, I. Bodrenko, A. Messina, H. Kmita, M. Ceccarelli, and V. De Pinto. (2018). yVDAC2, the second mitochondrial porin isoform of Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1859: 270-279. 29408701
Guarino, F., V. Specchia, G. Zapparoli, A. Messina, R. Aiello, M.P. Bozzetti, and V. De Pinto. (2006). Expression and localization in spermatozoa of the mitochondrial porin isoform 2 in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 346: 665-670. 16774740
Gupta, A. and R. Mahalakshmi. (2019). Helix-strand interaction regulates stability and aggregation of the human mitochondrial membrane protein channel VDAC3. J Gen Physiol. [Epub: Ahead of Print] 30674561
Hiller, S., J. Abramson, C. Mannella, G. Wagner, and K. Zeth. (2010). The 3D structures of VDAC represent a native conformation. Trends. Biochem. Sci. 35: 514-521. 20708406
Hiller, S., R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, and G. Wagner. (2008). Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321: 1206-1210. 18755977
Israelson, A., N. Arbel, S. Da Cruz, H. Ilieva, K. Yamanaka, V. Shoshan-Barmatz, and D.W. Cleveland. (2010). Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron. 67: 575-587. 20797535
Jeanteur, D., J.H. Lakey, and F. Pattus. (1991). The bacterial porin superfamily: sequence alignment and structure prediction. Mol. Microbiol. 5: 2153-2164. 1662760
Jeanteur, D., J.H. Lakey, and F. Pattus. (1994). The porin superfamily: diversity and common features. In Bacterial Cell Wall, J.M. Ghuysen and R. Hakenbeck (Eds.), Amsterdam, Elsevier, pp. 363-380.
Kojima, S., M. Iwamoto, S. Oiki, S. Tochigi, and H. Takahashi. (2018). Thylakoid membranes contain a non-selective channel permeable to small organic molecules. J. Biol. Chem. 293: 7777-7785. 29602906
Lawen, A., J.D. Ly, D.J. Lane, K. Zarschler, A. Messina, and V. De Pinto. (2005). Voltage-dependent anion-selective channel 1 (VDAC1)--a mitochondrial protein, rediscovered as a novel enzyme in the plasma membrane. Int J Biochem. Cell Biol. 37: 277-282. 15474974
Leung, A.W. and A.P. Halestrap. Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochim. Biophys. Acta. 1777: 946-952. 18407825
Ludwig, O., R. Benz, and J.E. Schultz. (1989). Porin of Paramecium mitochondria isolation, characterization and ion selectivity of the closed state. Biochim. Biophys. Acta. 978: 319-327. 2536559
Makiuchi, T., F. Mi-ichi, K. Nakada-Tsukui, and T. Nozaki. (2013). Novel TPR-containing subunit of TOM complex functions as cytosolic receptor for Entamoeba mitosomal transport. Sci Rep 3: 1129. 23350036
Makki, A., P. Rada, V. Žárský, S. Kereïche, L. Kováčik, M. Novotný, T. Jores, D. Rapaport, and J. Tachezy. (2019). Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis. PLoS Biol 17: e3000098. 30608924
Maurya, S.R. and R. Mahalakshmi. (2014). Cysteine Residues Impact the Stability and Micelle Interaction Dynamics of the Human Mitochondrial β-Barrel Anion Channel hVDAC-2. PLoS One 9: e92183. 24642864
Maurya, S.R. and R. Mahalakshmi. (2014). Influence of protein-micelle ratios and cysteine residues on the kinetic stability and unfolding rates of human mitochondrial VDAC-2. PLoS One 9: e87701. 24494036
Maurya, S.R. and R. Mahalakshmi. (2015). VDAC-2: Mitochondrial outer membrane regulator masquerading as a channel? FEBS J. [Epub: Ahead of Print] 26709731
Messina, A., S. Reina, F. Guarino, and V. De Pinto. (2012). VDAC isoforms in mammals. Biochim. Biophys. Acta. 1818: 1466-1476. 22020053
Miyata, N., S. Fujii, and O. Kuge. (2018). Porin proteins have critical functions in mitochondrial phospholipid metabolism in yeast. J. Biol. Chem. [Epub: Ahead of Print] 30237174
Naghdi, S., P. Várnai, and G. Hajnóczky. (2015). Motifs of VDAC2 required for mitochondrial Bak import and tBid-induced apoptosis. Proc. Natl. Acad. Sci. USA 112: E5590-5599. 26417093
Nikaido, H. (1992). Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6: 435-442. 1373213
Pan, X., Z. Chen, X. Yang, and G. Liu. (2014). Arabidopsis Voltage-Dependent Anion Channel 1 (AtVDAC1) Is Required for Female Development and Maintenance of Mitochondrial Functions Related to Energy-Transaction. PLoS One 9: e106941. 25192453
Rauch, G. and O. Moran. (1994). On the structure of mitochondrial porins and its homologies with bacterial porins. Biochem. Biophys. Res. Commun. 200: 908-915. 8179626
Reina, S., V. Checchetto, R. Saletti, A. Gupta, D. Chaturvedi, C. Guardiani, F. Guarino, M.A. Scorciapino, A. Magrì, S. Foti, M. Ceccarelli, A.A. Messina, R. Mahalakshmi, I. Szabo, and V. De Pinto. (2016). VDAC3 as a sensor of oxidative state of the intermembrane space of mitochondria: the putative role of cysteine residue modifications. Oncotarget 7: 2249-2268. 26760765
Röhl, T., M. Motzkus, and J. Soll. (1999). The outer envelope protein OEP24 from pea chloroplasts can functionally replace the mitochondrial VDAC in yeast. FEBS Lett. 460: 491-494. 10556523
Roosens, N., F. Al Bitar, M. Jacobs, and F. Homblé. (2000). Characterization of a cDNA encoding a rice mitochondrial voltage-dependent anion channel and its gene expression studied upon plant development and osmotic stress. Biochim. Biophys. Acta 1463: 470-476. 10675523
Saletti, R., S. Reina, M.G.G. Pittalà, A. Magrì, V. Cunsolo, S. Foti, and V. De Pinto. (2018). Post-translational modifications of VDAC1 and VDAC2 cysteines from rat liver mitochondria. Biochim. Biophys. Acta. [Epub: Ahead of Print] 29890122
Santos, H.J., K. Imai, Y. Hanadate, Y. Fukasawa, T. Oda, F. Mi-Ichi, and T. Nozaki. (2016). Screening and discovery of lineage-specific mitosomal membrane proteins in Entamoeba histolytica. Mol Biochem Parasitol 209: 10-17. 26792249
Sbidian E., Eftekahri P., Viguier M., Laroche L., Chosidow O., Gosselin P., Trouche F., Bonnet N., Arfi C., Tubach F. and Bachelez H. (201). National survey of psoriasis flares after 2009 monovalent H1N1/seasonal vaccines. Dermatology. 229(2):130-5. 25171322
Schulz, G.E. (1996). Porins: general to specific, native to engineered passive pores. Curr. Opin. Struc. Biol. 6: 485-490. 8794162
Shoshan-Barmatz, V., D. Ben-Hail, L. Admoni, Y. Krelin, and S.S. Tripathi. (2015). The mitochondrial voltage-dependent anion channel 1 in tumor cells. Biochim. Biophys. Acta. 1848: 2547-2575. 25448878
Shoshan-Barmatz, V., E. Nahon-Crystal, A. Shteinfer-Kuzmine, and R. Gupta. (2018). VDAC1, mitochondrial dysfunction, and Alzheimer''s disease. Pharmacol Res 131: 87-101. [Epub: Ahead of Print] 29551631
Shoshan-Barmatz, V., Y. Krelin, A. Shteinfer-Kuzmine, and T. Arif. (2017). Voltage-Dependent Anion Channel 1 As an Emerging Drug Target for Novel Anti-Cancer Therapeutics. Front Oncol 7: 154. 28824871
Shuvo, S.R., F.G. Ferens, and D.A. Court. (2016). The N-terminus of VDAC: Structure, mutational analysis, and a potential role in regulating barrel shape. Biochim. Biophys. Acta. [Epub: Ahead of Print] 26997586
Song, J., C. Midson, E. Blachly-Dyson, M. Forte, and M. Colombini. (1998). The topology of VDAC as probed by biotin modification. J. Biol. Chem. 273: 24406-24413. 9733730
Specchia, V., F. Guarino, A. Messina, M.P. Bozzetti, and V. De Pinto. (2008). Porin isoform 2 has a different localization in Drosophila melanogaster ovaries than porin 1. J. Bioenerg. Biomembr. 40: 219-226. 18686020
Sridharan M., Bowles EA., Richards JP., Krantic M., Davis KL., Dietrich KA., Stephenson AH., Ellsworth ML. and Sprague RS. (2012). Prostacyclin receptor-mediated ATP release from erythrocytes requires the voltage-dependent anion channel. Am J Physiol Heart Circ Physiol. 302(3):H553-9. 22159995
Srivastava, S.R., P. Zadafiya, and R. Mahalakshmi. (2018). Hydrophobic Mismatch Modulates Stability and Plasticity of Human Mitochondrial VDAC2. Biophys. J. [Epub: Ahead of Print] 30503532
Teixeira, J., C. Oliveira, F. Cagide, R. Amorim, J. Garrido, F. Borges, and P.J. Oliveira. (2018). Discovery of a new mitochondria permeability transition pore (mPTP) inhibitor based on gallic acid. J Enzyme Inhib Med Chem 33: 567-576. 29513043
Troll, H., D. Malchow, A. Müller-Taubenberger, B. Humbel, F. Lottspeich, M. Ecke, G. Gerisch, A. Schmid, and R. Benz. (1992). Purification, functional characterization, and cDNA sequencing of mitochondrial porin from Dictyostelium discoideum. J. Biol. Chem. 267: 21072-21079. 1328220
Ujwal, R., D. Cascio, J.P. Colletier, S. Faham, J. Zhang, L. Toro, P. Ping, and J. Abramson. (2008). The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. USA 105: 17742-17747. 18988731
Wojtkowska, M., M. Jąkalski, J.R. Pieńkowska, O. Stobienia, A. Karachitos, T.M. Przytycka, J. Weiner, 3rd, H. Kmita, and W. Makałowski. (2012). Phylogenetic analysis of mitochondrial outer membrane β-barrel channels. Genome Biol Evol 4: 110-125. 22155732
Yagoda N., M. von Rechenberg, E. Zaganjor, A.J. Bauer, W.S. Yang, D.J. Fridman, A.J. Wolpaw, I. Smukste, J.M. Peltier, J.J. Boniface, R. SmitH, S.L. Lessnick, S. Sahasrabudhe, B.R. Stockwell. (2007). RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature. 447: 864-868 17568748
Yehezkel, G., Hadad, N., Zaid, H., Sivan, S., and Shoshan-Barmatz, V. (2006). Nucleotide-binding sites in the voltage-dependent anion channel: characterization and localization. J. Biol. Chem. 281: 5938-5946. 16354668
Zeth, K. (2010). Structure and evolution of mitochondrial outer membrane proteins of β-barrel topology. Biochim. Biophys. Acta. 1797: 1292-1299. 20450883
Zhang, E., I. Mohammed Al-Amily, S. Mohammed, C. Luan, O. Asplund, M. Ahmed, Y. Ye, D. Ben-Hail, A. Soni, N. Vishnu, P. Bompada, Y. De Marinis, L. Groop, V. Shoshan-Barmatz, E. Renström, C.B. Wollheim, and A. Salehi. (2018). Preserving Insulin Secretion in Diabetes by Inhibiting VDAC1 Overexpression and Surface Translocation in β Cells. Cell Metab. [Epub: Ahead of Print] 30293774