Cysteine residues impact the stability and micelle interaction dynamics of the human mitochondrial β-barrel anion channel hVDAC-2

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Maurya, Svetlana Rajkumar ^a   Mahalakshmi, Radhakrishnan ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH BHOPAL   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; HUMAN VOLTAGE DEPENDENT ANION CHANNEL ISOFORM 2 PROTEIN; MITOCHONDRIAL PROTEIN; UNCLASSIFIED DRUG; DIMETHYLAMINE; DODECYLDIMETHYLAMINE OXIDE; ISOPROTEIN; MICELLE; RECOMBINANT PROTEIN; TRYPTOPHAN; VDAC2 PROTEIN, HUMAN; VOLTAGE DEPENDENT ANION CHANNEL 2;

ARTICLE; BETA CHAIN; CELL INTERACTION; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; MICELLE; MITOCHONDRION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN UNFOLDING; WILD TYPE; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; CYSTEINE; DIMETHYLAMINES; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; MICELLES; MITOCHONDRIA; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN ISOFORMS; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; THERMODYNAMICS; TRYPTOPHAN; VOLTAGE-DEPENDENT ANION CHANNEL 2;

EID: 84898651852     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092183     Document Type: Article

References (71)

1. Colombini M, Mannella CA (2012) VDAC, the early days. Biochim Biophys Acta 1818: 1438-1443.
2. Colombini M (2012) VDAC structure, selectivity, and dynamics. Biochim Biophys Acta 1818: 1457-1465.
3. Blachly-Dyson E, Zambronicz EB, Yu WH, Adams V, McCabe ER, et al. (1993) Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependen (Pubitemid 23033582)
4. Messina A, Reina S, Guarino F, De Pinto V (2012) VDAC isoforms in mammals. Biochim Biophys Acta 1818: 1466-1476.
5. Colombini M (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 256-257: 107-115. (Pubitemid 38181239)
6. De Pinto V, Guarino F, Guarnera A, Messina A, Reina S, et al. (2010) Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim Biophys Acta 1797: 1268-1275.
7. Bayrhuber M, Meins T, Habeck M, Becker S, Giller K, et al. (2008) Structure of the human voltage-dependent anion channel. Proc Natl Acad Sci U S A 105: 15370-15375.
8. Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, et al. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321: 1206-1210.
9. Ujwal R, Cascio D, Colletier JP, Faham S, Zhang J, et al. (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci U S A 105: 17742-17747.
10. Bathori G, Szabo I, Schmehl I, Tombola F, Messina A, et al. (1998) Novel aspects of the electrophysiology of mitochondrial porin. Biochem Biophys Res Commun 243: 258-263. (Pubitemid 28414224)
11. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517. (Pubitemid 36900308)
12. Keinan N, Tyomkin D, Shoshan-Barmatz V (2010) Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol 30: 5698-5709.
13. Reddy PH (2013) Is the mitochondrial outermembrane protein VDAC1 therapeutic target for Alzheimer's disease? Biochim Biophys Acta 1832: 67-75.
14. Shoshan-Barmatz V, Golan M (2012) Mitochondrial VDAC1: function in cell life and death and a target for cancer therapy. Curr Med Chem 19: 714-735.
15. Maldonado EN, Sheldon KL, DeHart DN, Patnaik J, Manevich Y, et al. (2013) Voltage-dependent anion channels modulate mitochondrial metabolism in cancer cells: regulation by free tubulin and erastin. J Biol Chem 288: 11920-11929.
16. Yu TY, Raschle T, Hiller S, Wagner G (2012) Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim Biophys Acta 1818: 1562-1569.
17. Rostovtseva TK, Tan W, Colombini M (2005) On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 37: 129-142. (Pubitemid 41420468)
18. Ren D, Kim H, Tu HC, Westergard TD, Fisher JK, et al. (2009) The VDAC2-BAK rheostat controls thymocyte survival. Sci Signal 2: ra48.
19. Zhang X, Weng C, Li Y, Wang X, Jiang C, et al. (2012) Human Bop is a novel BH3-only member of the Bcl-2 protein family. Protein Cell 3: 790-801.
20. Yagoda N, von Rechenberg M, Zaganjor E, Bauer AJ, Yang WS, et al. (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447: 864-868. (Pubitemid 46920135)
21. Bauer AJ, Gieschler S, Lemberg KM, McDermott AE, Stockwell BR (2011) Functional model of metabolite gating by human voltage-dependent anion channel 2. Biochemistry 50: 3408-3410.
22. Aram L, Geula S, Arbel N, Shoshan-Barmatz V (2010) VDAC1 cysteine residues: topology and function in channel activity and apoptosis. Biochem J 427: 445-454.
23. Tomasello MF, Guarino F, Reina S, Messina A, De Pinto V (2013) The Voltage-Dependent Anion Selective Channel 1 (VDAC1) Topography in the Mitochondrial Outer Membrane as Detected in Intact Cell. PLoS One 8: e81522.
24. Maurya SR, Mahalakshmi R (2013) Modulation of Human Mitochondrial Voltage-dependent Anion Channel 2 (hVDAC-2) Structural Stability by Cysteine-assisted Barrel-lipid Interactions. J Biol Chem 288: 25584-25592.
25. Curnow P, Booth PJ (2007) Combined kinetic and thermodynamic analysis of alpha-helical membrane protein unfolding. Proc Natl Acad Sci U S A 104: 18970-18975.
26. Huysmans GH, Baldwin SA, Brockwell DJ, Radford SE (2010) The transition state for folding of an outer membrane protein. Proc Natl Acad Sci U S A 107: 4099-4104.
27. Moon CP, Kwon S, Fleming KG (2011) Overcoming hysteresis to attain reversible equilibrium folding for outer membrane phospholipase A in phospholipid bilayers. J Mol Biol 413: 484-494.
28. Moon CP, Zaccai NR, Fleming PJ, Gessmann D, Fleming KG (2013) Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc Natl Acad Sci U S A 110: 4285-4290.
29. Pocanschi CL, Popot JL, Kleinschmidt JH (2013) Folding and stability of outer membrane protein A (OmpA) from Escherichia coli in an amphipathic polymer, amphipol A8-35. Eur Biophys J 42: 103-118.
30. Schlebach JP, Peng D, Kroncke BM, Mittendorf KF, Narayan M, et al. (2013) Reversible folding of human peripheral myelin protein 22, a tetraspan membrane protein. Biochemistry 52: 3229-3241.
31. Jackson SE (1998) How do small single-domain proteins fold? Fold Des 3: R81-R91. (Pubitemid 28366044)
32. Sanchez-Ruiz JM (2010) Protein kinetic stability. Biophys Chem 148: 1-15.
33. Jefferson RE, Blois TM, Bowie JU (2013) Membrane proteins can have high kinetic stability. J Am Chem Soc 135: 15183-15190.
34. Maurya SR, Mahalakshmi R (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.
35. Mueller P, Rudin D, Tien H, Westcott W (1963) Methods for the Formation of Single Bimolecular Lipid Membranes in Aqueous Solution. J Phys Chem 67: 534-535.
36. Colombini M (2007) Measurement of VDAC permeability in intact mitochondria and in reconstituted systems. Methods Cell Biol 80: 241-260.
37. Maurya SR, Chaturvedi D, Mahalakshmi R (2013) Modulating lipid dynamics and membrane fluidity to drive rapid folding of a transmembrane barrel. Sci Rep 3: 1989 (DOI: 1910.1038/srep01989).
38. Eliceiri CAS, Wayne SR, Kevin W (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
39. Chaturvedi D, Mahalakshmi R (2013) Methionine Mutations of Outer Membrane Protein X Influence Structural Stability and beta-Barrel Unfolding. PLoS One 8: e79351.
40. Lakowicz JR (1991) Topics in Fluorescence Spectroscopy: Volume 2: Principles: Springer.
41. Moon CP, Fleming KG (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc Natl Acad Sci U S A 108: 10174-10177.
42. Myers JK, Pace CN, Scholtz JM (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci 4: 2138-2148.
43. Menzel VA, Cassara MC, Benz R, de Pinto V, Messina A, et al. (2009) Molecular and functional characterization of VDAC2 purified from mammal spermatozoa. Biosci Rep 29: 351-362.
44. Shanmugavadivu B, Apell HJ, Meins T, Zeth K, Kleinschmidt JH (2007) Correct folding of the beta-barrel of the human membrane protein VDAC requires a lipid bilayer. J Mol Biol 368: 66-78. (Pubitemid 46441214)
45. De Pinto V, Reina S, Guarino F, Messina A (2008) Structure of the voltage dependent anion channel: state of the art. J Bioenerg Biomembr 40: 139-147.
46. Herrmann KW (1962) Non-Ionic-Cationic Micellar Properties of Dimethyl-dodecylamine Oxide. J Phys Chem 66: 295-300.
47. Kleinschmidt JH, Wiener MC, Tamm LK (1999) Outer membrane protein A of E. coli folds into detergent micelles, but not in the presence of monomeric detergent. Protein Sci 8: 2065-2071. (Pubitemid 29489934)
48. Malia TJ, Wagner G (2007) NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL. Biochemistry 46: 514-525. (Pubitemid 46105440)
49. Zalk R, Israelson A, Garty ES, Azoulay-Zohar H, Shoshan-Barmatz V (2005) Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem J 386: 73-83. (Pubitemid 40289226)
50. Mudiyanselage APKKK, Yang M, Accomando LAR, Thompson LK, Weis RM (2013) Membrane Association of a Protein Increases the Rate, Extent, and Specificity of Chemical Cross-Linking. Biochemistry 52: 6127-6136.
51. Calhoun DB, Vanderkooi JM, Holtom GR, Englander SW (1986) Protein fluorescence quenching by small molecules: protein penetration versus solvent exposure. Proteins 1: 109-115.
52. Andersen KK, Wang H, Otzen DE (2012) A kinetic analysis of the folding and unfolding of OmpA in urea and guanidinium chloride: single and parallel pathways. Biochemistry 51: 8371-8383.
53. Findlay HE, Rutherford NG, Henderson PJ, Booth PJ (2010) Unfolding free energy of a two-domain transmembrane sugar transport protein. Proc Natl Acad Sci U S A 107: 18451-18456.
54. Greene RF, Jr., Pace CN (1974) Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. J Biol Chem 249: 5388-5393.
55. Ahmad F, Bigelow CC (1986) Estimation of the Stability of Globular-Proteins. Biopolymers 25: 1623-1633.
56. Neet KE, Timm DE (1994) Conformational stability of dimeric proteins: quantitative studies by equilibrium denaturation. Protein Sci 3: 2167-2174.
57. Sheshadri S, Lingaraju GM, Varadarajan R (1999) Denaturant mediated unfolding of both native and molten globule states of maltose binding protein are accompanied by large deltaCp's. Protein Sci 8: 1689-1695. (Pubitemid 29379951)
58. Kaufmann TC, Engel A, Remigy HW (2006) A novel method for detergent concentration determination. Biophys J 90: 310-317.
59. Strop P, Brunger AT (2005) Refractive index-based determination of detergent concentration and its application to the study of membrane proteins. Protein Sci 14: 2207-2211. (Pubitemid 41132386)
60. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344. (Pubitemid 37321833)
61. Franzin CM, Teriete P, Marassi FM (2007) Structural similarity of a membrane protein in micelles and membranes. J Am Chem Soc 129: 8078-8079. (Pubitemid 47035115)
62. Hiller S, Abramson J, Mannella C, Wagner G, Zeth K (2010) The 3D structures of VDAC represent a native conformation. Trends Biochem Sci 35: 514-521.
63. Stangl M, Veerappan A, Kroeger A, Vogel P, Schneider D (2012) Detergent properties influence the stability of the glycophorin A transmembrane helix dimer in lysophosphatidylcholine micelles. Biophys J 103: 2455-2464.
64. Tan EH, Birge RR (1996) Correlation between surfactant/micelle structure and the stability of bacteriorhodopsin in solution. Biophys J 70: 2385-2395. (Pubitemid 26133733)
65. Venkatesu P, Lee MJ, Lin HM (2007) Trimethylamine N-oxide counteracts the denaturing effects of urea or GdnHCl on protein denatured state. Arch Biochem Biophys 466: 106-115. (Pubitemid 47405073)
66. Canchi DR, Garcia AE (2013) Cosolvent effects on protein stability. Annu Rev Phys Chem 64: 273-293.
67. Kaufmann TC (2006) Detergent-protein and Detergent-lipid Interactions: Implications for Two-dimensional Crystallization of Membrane Proteins and Development of Tools for High Throughput Crystallography.
68. Horvath SE, Daum G (2013) Lipids of mitochondria. Prog Lipid Res 52: 590-614.
69. Plotz M, Gillissen B, Hossini AM, Daniel PT, Eberle J (2012) Disruption of the VDAC2-Bak interaction by Bcl-x(S) mediates efficient induction of apoptosis in melanoma cells. Cell Death Differ 19: 1928-1938.
70. Lazarou M, Stojanovski D, Frazier AE, Kotevski A, Dewson G, et al. (2010) Inhibition of Bak activation by VDAC2 is dependent on the Bak transmembrane anchor. J Biol Chem 285: 36876-36883.
71. Li Z, Wang Y, Xue Y, Li X, Cao H, et al. (2012) Critical role for voltage-dependent anion channel 2 in infectious bursal disease virus-induced apoptosis in host cells via interaction with VP5. J Virol 86: 1328-1338.