Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Towards understanding of plant mitochondrial VDAC proteins: an overview of bean (Phaseolus) VDAC proteins

1 Structure et Fonction des Membranes Biologiques, Université Libre de Bruxelles (ULB), Boulevard du Triomphe CP 206/2, B-1050 Brussels, Belgium
2 Laboratory of Bioenergetics, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland
3 I.R.P.H.E., Aix-Marseille Université, CNRS, Technopôle de Château-Gombert, F-13384, Marseille Cedex 13, France

Special Issues: BIOPHYSICS OF ION TRANSPORT IN PLANTS

As the main grain legume consumed worldwide, the common bean (Phaseolus vulgaris) is generally considered as a model for food legumes. The mitochondrial voltage-dependent anion-selective channel (VDAC) is the major transport pathway for inorganic ions, metabolites, and tRNA, and consequently it controls the exchange of these compounds between the cytoplasm and the mitochondrion. Two VDAC isoforms of Phaseolus coccineus have been investigated experimentally. However, plant VDACs are known to belong to a small multigenic family of variable size. Here, we combine available experimental as well as genomic and transcriptomic data to identify and characterize the VDAC family of Phaseolus vulgaris. To this aim, we review the current state of our knowledge of Phaseolus VDAC functional and structural properties. The genomic and transcriptomic data available for the putative VDACs of Phaseolus vulgaris are studied using bioinformatics approach including homology modelling. The obtained results indicate that five out of the seven putative VDAC encoding sequences (named PvVDAC1–5) share strongly conserved motifs and structural homology with known VDACs. Notably, PvVDAC4 and PvVDAC5 are very close to the two abundant and characterized experimentally VDAC isoforms purified from Phaseolus coccineus mitochondria.
  Figure/Table
  Supplementary
  Article Metrics

Keywords Phaseolus; mitochondria; VDAC; functional and structural properties

Citation: Hayet Saidani, Daria Grobys, Marc Léonetti, Hanna Kmita, Fabrice Homblé. Towards understanding of plant mitochondrial VDAC proteins: an overview of bean (Phaseolus) VDAC proteins. AIMS Biophysics, 2017, 4(1): 43-62. doi: 10.3934/biophy.2017.1.43

References

  • 1. Delgado-Salinas A, Bibler R, Lavin M (2006) Phylogeny of the genus phaseolus (leguminosae): a recent diversification in an ancient landscape. Syst Bot 31: 779–791.    
  • 2. Chacón S MI, Pickersgill B, Debouck DG, et al. (2007) Phylogeographic analysis of the chloroplast DNA variation in wild common bean (Phaseolus vulgaris L.) in the Americas. Plant Syst Evol 266: 175–195.    
  • 3. Parreira JR, Bouraada J, Fitzpatrick MA, et al. (2016) Differential proteomics reveals the hallmarks of seed development in common bean (Phaseolus vulgaris L.). J Proteomics 143: 188–198.    
  • 4. Woodstock LW, Pollock BM (1965) Physiological predetermination: imbibition, respiration, and growth of lima bean seeds. Science 150: 1031–1032.    
  • 5. Palmieri F, Agrimi G, Blanco E, et al. (2006) Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim Biophys Acta 1757: 1249–1262.
  • 6. Inoue I, Nagase H, Kishi K, et al. (1991) ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature 352: 244–247.    
  • 7. Siemen D, Loupatatzis C, Borecky J, et al. (1999) Ca2+-activated K channel of the BK-Type in the inner mitochondrial membrane of a human glioma cell line. Biochem Biophys Res Commun 257: 549–554.    
  • 8. Szabò I, Bock J, Jekle A, et al. (2005) A novel potassium channel in lymphocyte mitochondria. J Biol Chem 280: 12790–12798.    
  • 9. Pang K, Li Y, Liu M, et al. (2013) Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526: 411–428.    
  • 10. Srinivasan V, Pierik AJ, Lill R (2014) Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter atm1. Science 343: 1137–1140.    
  • 11. Homblé F, Krammer E-M, Prévost M (2012) Plant VDAC: Facts and speculations. Biochim Biophys Acta-Biomembr 1818: 1486–1501.    
  • 12. Marmagne A, Rouet M-A, Ferro M, et al. (2004) Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Mol Cell Proteomics 3: 675–691.    
  • 13. Robert N, D’Erfurth I, Marmagne A, et al. (2012) Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Mol Biol 78: 431–446.    
  • 14. De Pinto V, Messina A, Lane DJR, et al. (2010) Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Lett 584: 1793–1799.    
  • 15. Shoshan-Barmatz V, Pinto V De, Zweckstetter M, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227–285.    
  • 16. Baker MA, Lane DJR, Ly JD, et al. (2004) VDAC1 is a transplasma membrane NADH-ferricyanide reductase. J Biol Chem 279: 4811–4819.
  • 17. Parsons DF, Bonner J, Verboon JG (1965) Electron microscopy of isolated plant mitochondria and plastids using both the thin-section and the negative-staining techniques. Can J Bot 43: 647–655.    
  • 18. Mannella CA, Bonner WD (1975) X-ray diffraction from oriented outer mitochondrial membranes. Biochim Biophys Acta-Biomembr 413: 226–233.    
  • 19. Zalman LS, Nikaido H, Kagawa Y (1980) Mitochondrial outer membrane contains a protein producing nonspecific diffusion channels. J Biol Chem 255: 1771–1774.
  • 20. Schmutz J, McClean PE, Mamidi S, et al. (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46: 707–713.    
  • 21. Abrecht H, Wattiez R, Ruysschaert JM, et al. (2000) Purification and characterization of two voltage-dependent anion channel isoforms from plant seeds. Plant Physiol 124: 1181–1190.    
  • 22. Abrecht H, Goormaghtigh E, Ruysschaert JM, et al. (2000) Structure and orientation of two voltage-dependent anion-selective channel isoforms—An attenuated total reflection Fourier-transform infrared spectroscopy study. J Biol Chem 275: 40992–40999.    
  • 23. Homblé F, Mlayeh L, Léonetti M (2010) Planar lipid bilayers for electrophysiology of membrane-active peptides, In: Membr Pept Methods Results Struct Funct Electrophysiol, IUL: La Jolla, 273–307.
  • 24. Mlayeh L, Chatkaew S, Léonetti M, et al. (2010) Modulation of plant mitochondrial VDAC by phytosterols. Biophys J 99: 2097–2106.    
  • 25. Schein SJ, Colombini M, Finkelstein A (1976) Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J Membr Biol 30: 99–120.
  • 26. Rostovtseva TK, Colombini M (1996) ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane. J Biol Chem 271: 28006–28008.    
  • 27. Schmid A, Kromer S, Heldt HW, et al. (1992) Identification of two general diffusion channels in the outer membrane of pea mitochondria. Biochim Biophys Acta 1112: 174–180.    
  • 28. Heins L, Mentzel H, Schmid A, et al. (1994) Biochemical, molecular, and functional characterization of porin isoforms from potato mitochondria. J Biol Chem 269: 26402–26410.
  • 29. Blumenthal A, Kahn K, Beja O, et al. (1993) Purification and characterization of the voltage-dependent anion-selective channel protein from wheat mitochondrial membranes. Plant Physiol 101: 579–587.    
  • 30. Smack DP, Colombini M (1985) Voltage-dependent channels found in the membrane fraction of corn mitochondria. Plant Physiol 79: 1094–1097.
  • 31. Aljamal JA, Genchi G, De Pinto V, et al. (1993) Purification and characterization of porin from corn (Zea mays L.) mitochondria. Plant Physiol 102: 615–621.    
  • 32. Wunder UR, Colombini M (1991) Patch clamping VDAC in liposomes containing whole mitochondrial membranes. J Membr Biol 123: 83–91.    
  • 33. Levadny V, Colombini M, Li XX, et al. (2002) Electrostatics explains the shift in VDAC gating with salt activity gradient. Biophys J 82: 1773–1783.    
  • 34. Bayrhuber M, Meins T, Habeck M, et al. (2008) Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci USA 105: 15370–15375.    
  • 35. Hiller S, Garces RG, Malia TJ, et al. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321: 1206–1210.    
  • 36. Ujwal R, Cascio D, Colletier JP, et al. (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 105: 17742–17747.
  • 37. Schredelseker J, Paz A, Lopez CJ, et al. (2014) High resolution structure and double electron-electron resonance of the zebrafish voltage-dependent anion channel 2 reveal an oligomeric population. J Biol Chem 289: 12566–12577.    
  • 38. Schneider R, Etzkorn M, Giller K, et al. (2010) The native conformation of the human VDAC1 N terminus. Angew Chemie Int Ed 49: 1882–1885.    
  • 39. Guardiani C, Scorciapino MA, Amodeo GF, et al. (2015) The N-terminal peptides of the three human isoforms of the mitochondrial voltage-dependent anion channel have different helical propensities. Biochemistry 54: 5646–5656.    
  • 40. De Pinto V, Tomasello F, Messina A, et al. (2007) Determination of the conformation of the human VDAC1 N-terminal peptide, a protein moiety essential for the functional properties of the pore. Chem Bio Chem 8: 744–756.    
  • 41. Colombini M (2009) The published 3D structure of the VDAC channel: native or not? Trends Biochem Sci 34: 382–389.    
  • 42. Colombini M (2012) VDAC structure, selectivity, and dynamics. Biochim Biophys Acta-Biomembr 1818: 1457–1465.
  • 43. Lee K Il, Rui H, Pastor RW, et al. (2011) Brownian dynamics simulations of ion transport through the VDAC. Biophys J 100: 611–619.    
  • 44. Choudhary OP, Ujwal R, Kowallis W, et al. (2010) The electrostatics of VDAC: implications for selectivity and gating. J Mol Biol 396: 580–592.    
  • 45. Choudhary OP, Paz A, Adelman JL, et al. (2014) Structure-guided simulations illuminate the mechanism of ATP transport through VDAC1. Nat Struct Mol Biol 21: 626–632.    
  • 46. Hiller S, Abramson J, Mannella C, et al. (2010) The 3D structures of VDAC represent a native conformation. Trends Biochem Sci 35: 514–521.    
  • 47. Noskov SY, Rostovtseva TK, Bezrukov SM (2013) ATP Transport through VDAC and the VDAC-tubulin complex probed by equilibrium and nonequilibrium MD simulations. Biochemistry 52: 9246–9256.    
  • 48. Rui H, Lee K Il, Pastor RW, et al. (2011) Molecular dynamics studies of ion permeation in VDAC. Biophys J 100: 602–610.
  • 49. Young MJ, Bay DC, Hausner G, et al. (2007) The evolutionary history of mitochondrial porins. BMC Evol Biol 7: 31.    
  • 50. Kutik S, Stojanovski D, Becker L, et al. (2008) Dissecting membrane insertion of mitochondrial beta-barrel proteins. Cell 132: 1011–1024.
  • 51. Imai K, Fujita N, Gromiha MM, et al. (2011) Eukaryote-wide sequence analysis of mitochondrial beta-barrel outer membrane proteins. BMC Genomics 12: 79.    
  • 52. Jores T, Klinger A, Grosz LE, et al. (2016) Characterization of the targeting signal in mitochondrial [beta]-barrel proteins. Nat Commun 7.
  • 53. Shanmugavadivu B, Apell HJ, Meins T, et al. (2007) Correct folding of the beta-barrel of the human membrane protein VDAC requires a lipid bilayer. J Mol Biol 368: 66–78.    
  • 54. Shi Y, Jiang C, Chen Q, et al. (2003) One-step on-column affinity refolding purification and functional analysis of recombinant human VDAC1. Biochem Biophys Res Commun 303: 475–482.    
  • 55. Koppel DA, Kinnally KW, Masters P, et al. (1998) Bacterial expression and characterization of the mitochondrial outer membrane channel. Effects of n-terminal modifications. J Biol Chem 273: 13794–13800.
  • 56. Shao L, Kinnally KW, Mannella CA (1996) Circular dichroism studies of the mitochondrial channel, VDAC, from Neurospora crassa. Biophys J 71: 778–786.    
  • 57. Smeyers M, Léonetti M, Goormaghtigh E, et al. (2003) Structure and function of plant membrane ion channels reconstituted in planar lipid bilayers, In: Membr Sci Technol—Planar lipid bilayers their appl, Elsevier, 449–478.
  • 58. Villinger S, Briones R, Giller K, et al. (2010) Functional dynamics in the voltage-dependent anion channel. Proc Natl Acad Sci 107: 22546–22551.    
  • 59. Blachly-Dyson E, Peng S, Colombini M, et al. (1990) Selectivity changes in site-directed mutants of the VDAC ion channel: structural implications. Science 247: 1233–1236.    
  • 60. Zambrowicz EB, Colombini M (1993) Zero-current potentials in a large membrane channel: a simple theory accounts for complex behavior. Biophys J 65: 1093–1100.    
  • 61. Krammer E-M, Saidani H, Prévost M, et al. (2014) Origin of ion selectivity in Phaseolus coccineus VDAC mitochondrial channel. Mitochondrion 19B: 206–213.
  • 62. Rosenquist M, Sehnke P, Ferl RJ, et al. (2000) Evolution of the 14-3-3 protein family: does the large number of isoforms in multicellular organisms reflect functional specificity? J Mol Evol 51: 446–458.    
  • 63. Gasteiger E, Hoogland C, Gattiker A, et al. (2005) Protein identification and analysis tools on the ExPASy server, In: Walker JM, Proteomics Protoc, Totowa: Humana Press, 571–607
  • 64. Schleiff E, Eichacker LA, Eckart K, et al. (2003) Prediction of the plant beta-barrel proteome: A case study of the chloroplast outer envelope. Protein Sci 12: 748–759.    
  • 65. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33.
  • 66. Smith MD, Petrak M, Boucher PD, et al. (1995) Lysine residues at positions 234 and 236 in yeast porin are involved in its assembly into the mitochondrial outer membrane. J Biol Chem 270: 28331–28336.    
  • 67. Tateda C, Watanabe K, Kusano T, et al. (2011) Molecular and genetic characterization of the gene family encoding the voltage-dependent anion channel in Arabidopsis. J Exp Bot 62: 4773–4785.    
  • 68. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
  • 69. Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18: 6097–6100.    
  • 70. Crooks GE, Hon G, Chandonia J-M, et al. (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188–1190.    
  • 71. Biasini M, Bienert S, Waterhouse A, et al. (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42: W252–W258.    
  • 72. Yang Y, Faraggi E, Zhao H, et al. (2011) Improving protein fold recognition and template-based modeling by employing probabilistic-based matching between predicted one-dimensional structural properties of query and corresponding native properties of templates. Bioinformatics 27: 2076–2082.    

 

This article has been cited by

  • 1. Lamia Mlayeh, Eva-Maria Krammer, Marc Léonetti, Martine Prévost, Fabrice Homblé, The mitochondrial VDAC of bean seeds recruits phosphatidylethanolamine lipids for its proper functioning, Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2017, 1858, 9, 786, 10.1016/j.bbabio.2017.06.005

Reader Comments

your name: *   your email: *  

Copyright Info: 2017, Fabrice Homblé, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved