Voltage-dependent Anion Channel Isoform 3 As a Potential Male Contraceptive Drug Target

References

• Frankiewicz M , PolomW , MatuszewskiM. Can the evolution of male contraception lead to a revolution? Review of the current state of knowledge. Cent. European J. Urol.71(1), 108–113 (2018).
   PubMedGoogle Scholar
• Page ST , AmoryJK. Male hormonal contraceptive – are we there yet?Nat. Rev. Endocrinol.14(12), 685–686 (2018).
   PubMed Web of Science ®Google Scholar
• Behre HM , ZitzmannM , AndersonRAet al. Efficacy and safety of an injectable combination hormonal contraceptive for men. J. Clin. Endocrinol. Metab.101(12), 4779–4788 (2016).
   PubMed Web of Science ®Google Scholar
• Arifuzzaman S , RahmanMS , PangMG. Research update and opportunity of non-hormonal male contraception: histone demethylase KDM5B-based targeting. Pharmacol. Res.141, 1–20 (2018).
   PubMed Web of Science ®Google Scholar
• Pixton KL , DeeksED , FleschFMet al. Sperm proteome mapping of a patient who experienced failed fertilization at IVF reveals altered expression of at least 20 proteins compared with fertile donors: case report. Hum. Reprod.19(6), 1438–1447 (2004).
   PubMed Web of Science ®Google Scholar
• Li YF , HeW , MandalAet al. CABYR binds to AKAP3 and Ropporin in the human sperm fibrous sheath. Asian J. Androl.13(2), 266–274 (2011).
   PubMed Web of Science ®Google Scholar
• Miki K , QuW , GouldingEHet al. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc. Natl Acad. Sci. USA101(47), 16501–16506 (2004).
   PubMed Web of Science ®Google Scholar
• Tanaka H , IguchiN , ToyamaYet al. Mice deficient in the axonemal protein Tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol. Cell. Biol.24(18), 7958–7964 (2004).
   PubMed Web of Science ®Google Scholar
• Ferramosca A , ProvenzanoSP , CoppolaL , ZaraV. Mitochondrial respiratory efficiency is positively correlated with human sperm motility. Urology79(4), 809–814 (2012).
   PubMed Web of Science ®Google Scholar
• Paoli D , GalloM , RizzoFet al. Mitochondrial membrane potential profile and its correlation with increasing sperm motility. Fertil. Steril.95(7), 2315–2319 (2011).
   PubMed Web of Science ®Google Scholar
• Ruiz-Pesini E , LapenaAC , DiezC , AlvarezE , EnriquezJA , Lopez-PerezMJ. Seminal quality correlates with mitochondrial functionality. Clin. Chim. Acta300(1–2), 97–105 (2000).
   PubMed Web of Science ®Google Scholar
• Hereng TH , ElgstoenKB , CederkvistFHet al. Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum. Reprod.26(12), 3249–3263 (2011).
   PubMed Web of Science ®Google Scholar
• Piomboni P , FocarelliR , StendardiA , FerramoscaA , ZaraV. The role of mitochondria in energy production for human sperm motility. Int. J. Androl.35(2), 109–124 (2012).
   PubMedGoogle Scholar
• Colombini M . VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem.256–257(1–2), 107–115 (2004).
   PubMed Web of Science ®Google Scholar
• Rostovtseva TK , BezrukovSM. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenerg. Biomembr.40(3), 163–170 (2008).
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V , DePinto V , ZweckstetterM , RavivZ , KeinanN , ArbelN. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med.31(3), 227–285 (2010).
   PubMed Web of Science ®Google Scholar
• Tissue expression of VDAC3 - summary - The Human Protein Atlas (2018). www.proteinatlas.org/ENSG00000078668-VDAC3/tissue
   Google Scholar
• Raghavan A , SheikoT , GrahamBH , CraigenWJ. Voltage-dependant anion channels: novel insights into isoform function through genetic models. Biochim. Biophys. Acta1818(6), 1477–1485 (2012).
   PubMed Web of Science ®Google Scholar
• Anflous K , ArmstrongDD , CraigenWJ. Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J. Biol. Chem.276(3), 1954–1960 (2001).
   PubMed Web of Science ®Google Scholar
• Cheng EH , SheikoTV , FisherJK , CraigenWJ , KorsmeyerSJ. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science301(5632), 513–517 (2003).
   PubMed Web of Science ®Google Scholar
• Sampson MJ , DeckerWK , BeaudetALet al. Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel Type 3. J. Biol. Chem.276(42), 39206–39212 (2001).
   PubMed Web of Science ®Google Scholar
• Kwon WS , ParkYJ , Mohamedel SA , PangMG. Voltage-dependent anion channels are a key factor of male fertility. Fertil. Steril.99(2), 354–361 (2013).
   PubMed Web of Science ®Google Scholar
• Rostovtseva TK , BezrukovSM. VDAC inhibition by tubulin and its physiological implications. Biochim. Biophys. Acta1818(6), 1526–1535 (2012).
   PubMed Web of Science ®Google Scholar
• Lemasters JJ , HolmuhamedovE. Voltage-dependent anion channel (VDAC) as mitochondrial governator – thinking outside the box. Biochim. Biophys. Acta1762(2), 181–190 (2006).
   PubMed Web of Science ®Google Scholar
• Mannella CA , KinnallyKW. Reflections on VDAC as a voltage-gated channel and a mitochondrial regulator. J. Bioenerg. Biomembr.40(3), 149–155 (2008).
   PubMed Web of Science ®Google Scholar
• Galganska H , BudzinskaM , WojtkowskaM , KmitaH. Redox regulation of protein expression in Saccharomyces cerevisiae mitochondria: possible role of VDAC. Arch. Biochem. Biophys.479(1), 39–45 (2008).
   PubMed Web of Science ®Google Scholar
• Galganska H , KarachitosA , WojtkowskaM , StobieniaO , BudzinskaM , KmitaH. Communication between mitochondria and nucleus: putative role for VDAC in reduction/oxidation mechanism. Biochim. Biophys. Acta1797(6–7), 1276–1280 (2010).
   PubMed Web of Science ®Google Scholar
• McCommis KS , BainesCP. The role of VDAC in cell death: friend or foe?Biochim. Biophys. Acta1818(6), 1444–1450 (2012).
   PubMed Web of Science ®Google Scholar
• Messina A , ReinaS , GuarinoF , DePinto V. VDAC isoforms in mammals. Biochim. Biophys. Acta1818(6), 1466–1476 (2012).
   PubMed Web of Science ®Google Scholar
• De Pinto V , GuarinoF , GuarneraAet al. Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim. Biophys. Acta 1797(6–7), 1268–1275 (2010).
   PubMed Web of Science ®Google Scholar
• Hinsch KD , DePinto V , AiresVA , SchneiderX , MessinaA , HinschE. Voltage-dependent anion-selective channels VDAC2 and VDAC3 are abundant proteins in bovine outer dense fibers, a cytoskeletal component of the sperm flagellum. J. Biol. Chem.279(15), 15281–15288 (2004).
   PubMed Web of Science ®Google Scholar
• Majumder S , SlabodnickM , PikeA , MarquardtJ , FiskHA. VDAC3 regulates centriole assembly by targeting Mps1 to centrosomes. Cell Cycle11(19), 3666–3678 (2012).
   PubMed Web of Science ®Google Scholar
• Majumder S , FiskHA. VDAC3 and Mps1 negatively regulate ciliogenesis. Cell Cycle12(5), 849–858 (2013).
   PubMed Web of Science ®Google Scholar
• Checchetto V , ReinaS , MagriA , SzaboI , DePinto V. Recombinant human voltage dependent anion selective channel isoform 3 (hVDAC3) forms pores with a very small conductance. Cell. Physiol. Biochem.34(3), 842–853 (2014).
   PubMedGoogle Scholar
• Okazaki M , KurabayashiK , AsanumaM , SaitoY , DodoK , SodeokaM. VDAC3 gating is activated by suppression of disulfide-bond formation between the N-terminal region and the bottom of the pore. Biochim. Biophys. Acta1848(12), 3188–3196 (2015).
   PubMed Web of Science ®Google Scholar
• Xu X , DeckerW , SampsonMJ , CraigenWJ , ColombiniM. Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability. J. Membr. Biol.170(2), 89–102 (1999).
   PubMed Web of Science ®Google Scholar
• Karachitos A , GrobysD , AntoniewiczM , JedutS , JordanJ , KmitaH. Human VDAC isoforms differ in their capability to interact with minocycline and to contribute to its cytoprotective activity. Mitochondrion28, 38–48 (2016).
   PubMed Web of Science ®Google Scholar
• De Pinto V , ReinaS , GuptaA , MessinaA , MahalakshmiR. Role of cysteines in mammalian VDAC isoforms’ function. Biochim. Biophys. Acta1857(8), 1219–1227 (2016).
   PubMed Web of Science ®Google Scholar
• Reina S , ChecchettoV , SalettiRet al. VDAC3 as a sensor of oxidative state of the intermembrane space of mitochondria: the putative role of cysteine residue modifications. Oncotarget7(3), 2249–2268 (2016).
   PubMedGoogle Scholar
• Colombini M . The VDAC channel: molecular basis for selectivity. Biochim. Biophys. Acta1863(10), 2498–2502 (2016).
   PubMed Web of Science ®Google Scholar
• Stock CE , FraserLR. Divalent cations, capacitation and the acrosome reaction in human spermatozoa. J. Reprod. Fertil.87(2), 463–478 (1989).
   PubMedGoogle Scholar
• Freitas MJ , VijayaraghavanS , FardilhaM. Signaling mechanisms in mammalian sperm motility. Biol. Reprod.96(1), 2–12 (2017).
   PubMed Web of Science ®Google Scholar
• Liu B , TangM , HanZet al. Co-incubation of human spermatozoa with anti-VDAC antibody reduced sperm motility. Cell. Physiol. Biochem.33(1), 142–150 (2014).
   PubMedGoogle Scholar
• Liu B , WangP , WangZ , ZhangW. The use of anti-VDAC2 antibody for the combined assessment of human sperm acrosome integrity and ionophore A23187-induced acrosome reaction. PLoS ONE6(2), e16985 (2011).
   PubMed Web of Science ®Google Scholar
• Asmarinah , HinschKD , AiresVA , HinschE. Effect of anti-porin Type 2 antibodies upon bovine sperm motility and acrosomal status. Andrologia35(1), 2–3 (2003).
   Google Scholar
• Liu B , WangP , WangZet al. Analysis and difference of voltage-dependent anion channel mRNA in ejaculated spermatozoa from normozoospermic fertile donors and infertile patients with idiopathic asthenozoospermia. J. Assist. Reprod. Genet.27(12), 719–724 (2010).
   PubMed Web of Science ®Google Scholar
• Asmarinah , NurainiT , SumarsihTet al. Mutations in exons 5, 7 and 8 of the human voltage-dependent anion channel type 3 (VDAC3) gene in sperm with low motility. Andrologia44(1), 46–52 (2011).
   Web of Science ®Google Scholar
• Pan L , LiuQ , LiJet al. Association of the VDAC3 gene polymorphism with sperm count in Han-Chinese population with idiopathic male infertility. Oncotarget8(28), 45242–45248 (2017).
   PubMedGoogle Scholar
• Colombini M . Measurement of VDAC permeability in intact mitochondria and in reconstituted systems. Methods Cell. Biol.80, 241–260 (2007).
   PubMed Web of Science ®Google Scholar
• Lee AC , XuX , Blachly-DysonE , ForteM , ColombiniM. The role of yeast VDAC genes on the permeability of the mitochondrial outer membrane. J. Membr. Biol.161(2), 173–181 (1998).
   PubMed Web of Science ®Google Scholar
• Benz R . Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta1197(2), 167–196 (1994).
   PubMed Web of Science ®Google Scholar
• Zizi M , ForteM , Blachly-DysonE , ColombiniM. NADH regulates the gating of VDAC, the mitochondrial outer membrane channel. J. Biol. Chem.269(3), 1614–1616 (1994).
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG , ChandelNS , LiXX , SchumackerPT , ColombiniM , ThompsonCB. Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc. Natl Acad. Sci. USA97(9), 4666–4671 (2000).
   PubMed Web of Science ®Google Scholar
• Roman I , FigysJ , SteursG , ZiziM. Hunting interactomes of a membrane protein: obtaining the largest set of voltage-dependent anion channel-interacting protein epitopes. Mol. Cell. Proteomics5(9), 1667–1680 (2006).
   PubMed Web of Science ®Google Scholar
• Rostovtseva TK , AntonssonB , SuzukiM , YouleRJ , ColombiniM , BezrukovSM. Bid, but not Bax, regulates VDAC channels. J. Biol. Chem.279(14), 13575–13583 (2004).
   PubMed Web of Science ®Google Scholar
• Kmita H , BudzinskaM , StobieniaO. Modulation of the voltage-dependent anion-selective channel by cytoplasmic proteins from wild type and the channel depleted cells of Saccharomyces cerevisiae. Acta Biochim. Pol.50(2), 415–424 (2003).
   PubMed Web of Science ®Google Scholar
• Stobienia O , WroblewskaS , AntosN , BudzinskaM , KmitaH. The key role of the energized state of Saccharomyces cerevisiae mitochondria in modulations of the outer membrane channels by the intermembrane space proteins. J. Bioenerg. Biomembr.34(6), 507–516 (2002).
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V , Ben-HailD. VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion12(1), 24–34 (2012).
   PubMed Web of Science ®Google Scholar
• Park J , KimY , ChoiSet al. Drosophila Porin/VDAC affects mitochondrial morphology. PLoS ONE5(10), e13151 (2010).
   PubMed Web of Science ®Google Scholar
• Schwarzer C , Barnikol-WatanabeS , ThinnesFP , HilschmannN. Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int. J. Biochem. Cell. Biol.34(9), 1059–1070 (2002).
   PubMed Web of Science ®Google Scholar
• Karachitos A , JordanJ , KmitaH. VDAC-targeted drugs affecting cytoprotection and mitochondrial physiology in cerebrovascular and cardiovascular diseases. Curr. Med. Chem.24(40), 4419–4434 (2017).
   PubMed Web of Science ®Google Scholar
• Mazure NM . VDAC in cancer. Biochim. Biophys. Acta1858(8), 665–673 (2017).
   Web of Science ®Google Scholar
• Hoffmann EK . Anion exchange and anion-cation co-transport systems in mammalian cells. Philos. Trans. R Soc. Lond. B Biol. Sci.299(1097), 519–535 (1982).
   PubMed Web of Science ®Google Scholar
• Karachitos A , GarciaDel Pozo JS , de GrootPW , KmitaH , JordanJ. Minocycline mediated mitochondrial cytoprotection: premises for therapy of cerebrovascular and neurodegenerative diseases. Curr. Drug Targets14(1), 47–55 (2013).
   PubMed Web of Science ®Google Scholar
• Plane JM , ShenY , PleasureDE , DengW. Prospects for minocycline neuroprotection. Arch. Neurol.67(12), 1442–1448 (2010).
   PubMedGoogle Scholar
• Ahmad K , FooteRH. Postthaw survival and fertility of frozen bull spermatozoa treated with antibiotics and detergent. J. Dairy Sci.69(2), 535–541 (1986).
   PubMed Web of Science ®Google Scholar
• Schlegel PN , ChangTS , MarshallFF. Antibiotics: potential hazards to male fertility. Fertil. Steril.55(2), 235–242 (1991).
   PubMed Web of Science ®Google Scholar
• Malallah YA , ZissisNP. Effect of minocycline on the sperm count and activity in infertile men with high pus cell count in their seminal fluid. J. Chemother.4(5), 286–289 (1992).
   PubMed Web of Science ®Google Scholar
• White IG . The toxicity of some antibacterials for bull, ram, rabbit and human spermatozoa. Aust. J. Exp. Biol. Med. Sci.32(1), 41–48 (1954).
   PubMedGoogle Scholar
• Amin AH , BaileyJL , StoreyBT , BlascoL , HeynerS. A comparison of three methods for detecting the acrosome reaction in human spermatozoa. Hum. Reprod.11(4), 741–745 (1996).
   PubMed Web of Science ®Google Scholar
• Anflous-Pharayra K , LeeN , ArmstrongDL , CraigenWJ. VDAC3 has differing mitochondrial functions in two types of striated muscles. Biochim. Biophys. Acta1807(1), 150–156 (2011).
   PubMed Web of Science ®Google Scholar
• Zou L , LinckV , ZhaiYJet al. Knockout of mitochondrial voltage-dependent anion channel Type 3 increases reactive oxygen species (ROS) levels and alters renal sodium transport. J. Biol. Chem.293(5), 1666–1675 (2018).
   PubMed Web of Science ®Google Scholar
• Shamir R , KleinC , AmarDet al. Analysis of blood-based gene expression in idiopathic Parkinson disease. Neurology89(16), 1676–1683 (2017).
   PubMed Web of Science ®Google Scholar
• Sun Y , VashishtAA , TchieuJ , WohlschlegelJA , DreierL. Voltage-dependent anion channels (VDACs) recruit Parkin to defective mitochondria to promote mitochondrial autophagy. J. Biol. Chem.287(48), 40652–40660 (2012).
   PubMed Web of Science ®Google Scholar
• Springer W , KahlePJ. Regulation of PINK1-Parkin-mediated mitophagy. Autophagy7(3), 266–278 (2011).
   PubMed Web of Science ®Google Scholar
• Narendra D , KaneLA , HauserDN , FearnleyIM , YouleRJ. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy6(8), 1090–1106 (2010).
   PubMed Web of Science ®Google Scholar
• Meng XY , ZhangHX , MezeiM , CuiM. Molecular docking: a powerful approach for structure-based drug discovery. Curr. Comput. Aided Drug Des.7(2), 146–157 (2011).
   PubMed Web of Science ®Google Scholar
• Bayrhuber M , MeinsT , HabeckMet al. Structure of the human voltage-dependent anion channel. Proc. Natl Acad. Sci. USA105(40), 15370–15375 (2008).
   PubMed Web of Science ®Google Scholar
• Hiller S , GarcesRG , MaliaTJ , OrekhovVY , ColombiniM , WagnerG. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science321(5893), 1206–1210 (2008).
   PubMed Web of Science ®Google Scholar
• Schredelseker J , PazA , LopezCJet al. High resolution structure and double electron-electron resonance of the zebrafish voltage-dependent anion channel 2 reveal an oligomeric population. J. Biol. Chem.289(18), 12566–12577 (2014).
   PubMed Web of Science ®Google Scholar
• Ujwal R , CascioD , ColletierJPet al. The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc. Natl Acad. Sci. USA105(46), 17742–17747 (2008).
   PubMed Web of Science ®Google Scholar
• Dixon SJ , StockwellBR. Identifying druggable disease-modifying gene products. Curr. Opin. Chem. Biol.13(5–6), 549–555 (2009).
   PubMed Web of Science ®Google Scholar
• Rahman MS , LeeJS , KwonWS , PangMG. Sperm proteomics: road to male fertility and contraception. Int. J. Endocrinol.2013, 360986 (2013).
   PubMed Web of Science ®Google Scholar