Combining nano-differential scanning fluorimetry and microscale thermophoresis to investigate VDAC1 interaction with small molecules

References

• Magrì A, Di Rosa MC, Orlandi I, et al. Deletion of Voltage-Dependent Anion Channel 1 knocks mitochondria down triggering metabolic rewiring in yeast. Cell Mol Life Sci. 2020;77:3195–213.
   PubMed Web of Science ®Google Scholar
• Rosencrans WM, Rajendran M, Bezrukov SM, Rostovtseva TK. VDAC regulation of mitochondrial calcium flux: from channel biophysics to disease. Cell Calcium 2021;94:102356.
   PubMed Web of Science ®Google Scholar
• Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004;256:107–15.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, Maldonado EN, Krelin Y. VDAC1 at the crossroads of cell metabolism, apoptosis and cell stress. Cell Stress 2017;1:11–36.
   PubMedGoogle Scholar
• Keinan N, Tyomkin D, Shoshan-Barmatz V. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol 2010;30:5698–709.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, De Pinto V, Zweckstetter M, et al. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 2010;31:227–85.
   PubMed Web of Science ®Google Scholar
• Hosaka T, Okazaki M, Kimura-Someya T, et al. Crystal structural characterization reveals novel oligomeric interactions of human voltage-dependent anion channel 1: Novel Oligomeric Structure of Human VDAC1. Protein Sci 2017;26:1749–58.
   PubMed Web of Science ®Google Scholar
• Huang L, Han J, Ben-Hail D, et al. A new fungal diterpene induces VDAC1-dependent apoptosis in Bax/Bak-deficient cells. J Biol Chem 2015;290:23563–78.
   PubMed Web of Science ®Google Scholar
• Tajeddine N, Galluzzi L, Kepp O, et al. Hierarchical involvement of Bak, VDAC1 and Bax in cisplatin-induced cell death. Oncogene 2008;27:4221–32.
   PubMed Web of Science ®Google Scholar
• Arbel N, Ben-Hail D, Shoshan-Barmatz V. Mediation of the antiapoptotic activity of Bcl-xL protein upon interaction with VDAC1 protein. J Biol Chem 2012;287:23152–61.
   PubMed Web of Science ®Google Scholar
• Azoulay-Zohar H, Israelson A, Abu-Hamad S, Shoshan-Barmatz V. In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem J 2004;377:347–55.
   PubMed Web of Science ®Google Scholar
• Rosano C. Molecular model of hexokinase binding to the outer mitochondrial membrane porin (VDAC1): implication for the design of new cancer therapies. Mitochondrion 2011;11:513–9.
   PubMed Web of Science ®Google Scholar
• Geula S, Ben-Hail D, Shoshan-Barmatz V. Structure-based analysis of VDAC1: N-terminus location, translocation, channel gating and association with anti-apoptotic proteins. Biochem J 2012;444:475–85.
   PubMed Web of Science ®Google Scholar
• Hiller S, Garces RG, Malia TJ, et al. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008;321:1206–10.
   PubMed Web of Science ®Google Scholar
• Bayrhuber M, Meins T, Habeck M, et al. Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci 2008;105:15370–5.
   PubMed Web of Science ®Google Scholar
• Ujwal R, Cascio D, Colletier J-P, et al. The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci 2008;105:17742–7.
   PubMed Web of Science ®Google Scholar
• Najbauer EE, Becker S, Giller K, et al. Structure, gating and interactions of the voltage-dependent anion channel. Eur Biophys J 2021;50:159–72.
   PubMed Web of Science ®Google Scholar
• Colombini M. Voltage gating in the mitochondrial channel, VDAC. J Membr Biol 1989;111:103–11.
   PubMed Web of Science ®Google Scholar
• Preto J, Gorny H, Krimm I. A deep dive into VDAC1 conformational diversity using all-atom simulations provides new insights into the structural origin of the closed states. Int J Mol Sci 2022;23:1175.
   PubMed Web of Science ®Google Scholar
• Mertins B, Psakis G, Grosse W, et al. Flexibility of the N-terminal mVDAC1 segment controls the channel’s gating behavior zhang Z, editor. PLoS ONE 2012;7:e47938.
   PubMed Web of Science ®Google Scholar
• Abu-Hamad S, Arbel N, Calo D, et al. The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J Cell Sci 2009;122:1906–16.
   PubMed Web of Science ®Google Scholar
• Arrowsmith CH, Audia JE, Austin C, et al. The promise and peril of chemical probes. Nat Chem Biol 2015;11:536–41.
   PubMed Web of Science ®Google Scholar
• Reina S, De Pinto V. Anti-cancer compounds targeted to VDAC: potential and perspectives. Curr Med Chem 2017;24:4447–69.
   PubMed Web of Science ®Google Scholar
• Tewari D, Majumdar D, Vallabhaneni S, Bera AK. Aspirin induces cell death by directly modulating mitochondrial voltage-dependent anion channel (VDAC). Sci Rep 2017;7:45184.
   PubMed Web of Science ®Google Scholar
• Tewari D, Ahmed T, Chirasani VR, et al. Modulation of the mitochondrial voltage dependent anion channel (VDAC) by curcumin. Biochim Biophys Acta (BBA) - Biomembr 2015;1848:151–8.
   PubMed Web of Science ®Google Scholar
• Arif T, Krelin Y, Nakdimon I, et al. VDAC1 is a molecular target in glioblastoma, with its depletion leading to reprogrammed metabolism and reversed oncogenic properties. Neuro-Oncology 2017;19:951–64.
   PubMed Web of Science ®Google Scholar
• Israelson A, Zaid H, Abu-Hamad S, et al. Mapping the ruthenium red-binding site of the voltage-dependent anion channel-1. Cell Calcium 2008;43:196–204.
   PubMed Web of Science ®Google Scholar
• Heslop KA, Burger P, Kappler C, et al. Small molecules targeting the NADH-binding pocket of VDAC modulate mitochondrial metabolism in hepatocarcinoma cells. Biomed Pharmacother 2022;150:112928.
   PubMed Web of Science ®Google Scholar
• Ben-Hail D, Begas-Shvartz R, Shalev M, et al. Novel compounds targeting the mitochondrial protein VDAC1 inhibit apoptosis and protect against mitochondrial dysfunction. J Biol Chem 2016;291:24986–5003.
   PubMed Web of Science ®Google Scholar
• Zhang E, Mohammed Al-Amily I, Mohammed S, et al. Preserving insulin secretion in diabetes by inhibiting VDAC1 overexpression and surface translocation in β cells. Cell Metabol 2019;29:64–77.e6.
   PubMed Web of Science ®Google Scholar
• Kim J, Gupta R, Blanco LP, et al. VDAC oligomers form mitochondrial pores to release mtDNA fragments and promote lupus-like disease. Science 2019;366:1531–6.
   PubMed Web of Science ®Google Scholar
• Verma A, Pittala S, Alhozeel B, et al. The role of the mitochondrial protein VDAC1 in inflammatory bowel disease: a potential therapeutic target. Mol Ther 2022;30:726–44.
   PubMed Web of Science ®Google Scholar
• Li Q, Qiao P, Chen X, et al. Affinity chromatographic methodologies based on immobilized voltage dependent anion channel isoform 1 and application in protein-ligand interaction analysis and bioactive compounds screening from traditional medicine. J Chromatogr A 2017;1495:31–45.
   PubMed Web of Science ®Google Scholar
• Rimmerman N, Ben-Hail D, Porat Z, et al. Direct modulation of the outer mitochondrial membrane channel, voltage-dependent anion channel 1 (VDAC1) by cannabidiol: a novel mechanism for cannabinoid-induced cell death. Cell Death Dis 2013;4:e949.
   PubMed Web of Science ®Google Scholar
• Head SA, Shi W, Zhao L, et al. Antifungal drug itraconazole targets VDAC1 to modulate the AMPK/mTOR signaling axis in endothelial cells. Proc Natl Acad Sci 2015;112:E7276–85.
   PubMed Web of Science ®Google Scholar
• Clémençon B, Fine M, Hediger MA. Conservation of the oligomeric state of native VDAC1 in detergent micelles. Biochimie 2016;127:163–72.
   PubMed Web of Science ®Google Scholar
• Yagoda N, von Rechenberg M, Zaganjor E, et al. RAS–RAF–MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 2007;447:865–9.
   Web of Science ®Google Scholar
• Böhm R, Amodeo GF, Murlidaran S, et al. The structural basis for low conductance in the membrane protein VDAC upon β-NADH binding and voltage gating. Structure (London, England: 1993). 2020;28:206–14.e4.
   PubMed Web of Science ®Google Scholar
• Silvers R, Eddy M. NMR spectroscopic studies of ion channels in lipid bilayers: sample preparation strategies exemplified by the voltage dependent anion channel. Methods Mol Biol 2021;2302:201–17.
   PubMedGoogle Scholar
• Magrì A, Reina S, De Pinto V. VDAC1 as pharmacological target in cancer and neurodegeneration: focus on its role in apoptosis. Front Chem 2018;6:108.
   PubMed Web of Science ®Google Scholar
• Olivas-Aguirre M, Torres-López L, Pottosin I, Dobrovinskaya O. Phenolic compounds cannabidiol, curcumin and quercetin cause mitochondrial dysfunction and suppress acute lymphoblastic leukemia cells. Int J Mol Sci 2020;22:204.
   PubMed Web of Science ®Google Scholar
• Weiser BP, Bu W, Wong D, Eckenhoff RG. Sites and functional consequence of VDAC-alkylphenol anesthetic interactions. FEBS Lett 2014;588:4398–403.
   PubMed Web of Science ®Google Scholar
• Weber JJ, Clemensson LE, Schiöth HB, Nguyen HP. Olesoxime in neurodegenerative diseases: Scrutinising a promising drug candidate. Biochem Pharmacol 2019;168:305–18.
   PubMed Web of Science ®Google Scholar
• Pinto VD, Al Jamal JA, Palmieri F. Location of the dicyclohexylcarbodiimide-reactive glutamate residue in the bovine heart mitochondrial porin. J Biol Chem 1993;268:12977–82.
   PubMed Web of Science ®Google Scholar
• Hill AP, Sitsapesan R. DIDS modifies the conductance, gating, and inactivation mechanisms of the cardiac ryanodine receptor. Biophys J 2002;82:3037–47.
   PubMed Web of Science ®Google Scholar
• Villinger S, Briones R, Giller K, et al. Functional dynamics in the voltage-dependent anion channel. Proc Natl Acad Sci 2010;107:22546–51.
   PubMed Web of Science ®Google Scholar
• Zaid H, Abu-Hamad S, Israelson A, et al. The voltage-dependent anion channel-1 modulates apoptotic cell death. Cell Death & Differ 2005;12:751–60.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, Hadad N, Feng W, et al. VDAC/porin is present in sarcoplasmic reticulum from skeletal muscle. FEBS Lett 1996;386:205–10.
   PubMed Web of Science ®Google Scholar
• Ben-Hail D, Shoshan-Barmatz V. VDAC1-interacting anion transport inhibitors inhibit VDAC1 oligomerization and apoptosis. Biochim Biophys Acta (BBA) - Mol Cell Res 2016;1863:1612–23.
   PubMed Web of Science ®Google Scholar
• Thinnes FP. Does fluoxetine (Prozak) block mitochondrial permeability transition by blocking VDAC as part of permeability transition pores? Mol Genet Metabol 2005;84:378.
   PubMed Web of Science ®Google Scholar
• Nahon E, Israelson A, Abu-Hamad S, Shoshan-Barmatz V. Fluoxetine (Prozac) interaction with the mitochondrial voltage-dependent anion channel and protection against apoptotic cell death. FEBS Letters 2005;579:5105–10.
   PubMed Web of Science ®Google Scholar
• Zizi M, Forte M, Blachly-Dyson E, Colombini M. NADH regulates the gating of VDAC, the mitochondrial outer membrane channel. J Biol Chem 1994;269:1614–6.
   PubMed Web of Science ®Google Scholar
• Rovini A, Gurnev PA, Beilina A, et al. Molecular mechanism of olesoxime-mediated neuroprotection through targeting α-synuclein interaction with mitochondrial VDAC. Cell Mol Life Sci CMLS 2020;77:3611–26.
   PubMed Web of Science ®Google Scholar
• Weiser BP, Kelz MB, Eckenhoff RG. In vivo activation of azipropofol prolongs anesthesia and reveals synaptic targets. J Biol Chem 2013;288:1279–85.
   PubMed Web of Science ®Google Scholar
• Malik C, Ghosh S. Quinidine partially blocks mitochondrial voltage-dependent anion channel (VDAC). Eur Biophys J 2020;49:193–205.
   PubMed Web of Science ®Google Scholar
• Murai M, Okuda A, Yamamoto T, et al. Synthetic ubiquinones specifically bind to mitochondrial voltage-dependent anion channel 1 (VDAC1) in Saccharomyces cerevisiae mitochondria. Biochemistry 2017;56:570–81.
   PubMed Web of Science ®Google Scholar
• Yang H-L, Tsai C-H, Shrestha S, et al. Coenzyme Q0, a novel quinone derivative of Antrodia camphorata, induces ROS-mediated cytotoxic autophagy and apoptosis against human glioblastoma cells in vitro and in vivo. Food Chem Toxicol 2021;155:112384.
   PubMed Web of Science ®Google Scholar
• Real-Hohn A, Groznica M, Löffler N, et al. nanoDSF: In vitro label-free method to monitor picornavirus uncoating and test compounds affecting particle stability. Front Microbiol 2020;11:1442.
   PubMed Web of Science ®Google Scholar
• Kim SH, Yoo HJ, Park EJ, Na DH. Nano differential scanning fluorimetry-based thermal stability screening and optimal buffer selection for immunoglobulin G. Pharmaceuticals 2021;15:29.
   Web of Science ®Google Scholar
• Queralt-Martín M, Bergdoll L, Teijido O, et al. A lower affinity to cytosolic proteins reveals VDAC3 isoform-specific role in mitochondrial biology. J General Physiol 2020;152:e201912501.
   PubMed Web of Science ®Google Scholar
• Wienken CJ, Baaske P, Rothbauer U, et al. Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 2010;1:100.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, Shteinfer-Kuzmine A, Verma A. VDAC1 at the intersection of cell metabolism, apoptosis, and diseases. Biomolecules 2020;10:1485. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693975/ [accessed 4 Jan 2021]
   PubMed Web of Science ®Google Scholar
• Puhl AC, Lane TR, Vignaux PA, et al. Computational approaches to identify molecules binding to Mycobacterium tuberculosis KasA. ACS Omega 2020;5:29935–42.
   PubMed Web of Science ®Google Scholar
• Solioz M. Dicyclohexylcarbodiimide as a probe for proton translocating enzymes. Trends Biochem Sci 1984;9:309–12.
   Google Scholar
• Horn JR, Shoichet BK. Allosteric inhibition through core disruption. J Mol Biol 2004;336:1283–91.
   PubMed Web of Science ®Google Scholar