Functional refolding and characterization of Two Tom40 isoforms from human mitochondria

Journal of Membrane Biology

Volumn 242, Issue 1, 2011, Pages 11-21

  Mager, Frauke ^a,b   Gessmann, Dennis ^a   Nussberger, Stephan ^a   Zeth, Kornelius ^b  

^a UNIVERSITY OF STUTTGART   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

barrel protein; Mitochondria; Protein conducting channel; Refolding; Tom40

Indexed keywords

ION CHANNEL; ISOPROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN TOM40A; PROTEIN TOM40B; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; HUMAN; LIPID BILAYER; MITOCHONDRIAL MEMBRANE; NEUROSPORA CRASSA; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN REFOLDING; PROTEIN STRUCTURE; PROTEIN VARIANT; THERMOSTABILITY;

CIRCULAR DICHROISM; ELECTROPHYSIOLOGY; HUMANS; LIPID BILAYERS; MITOCHONDRIAL PROTEINS; PROTEIN FOLDING; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

NEUROSPORA CRASSA;

EID: 79960574201     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-011-9372-8     Document Type: Article

References (45)

1. S Abu-Hamad N Arbel D Calo L Arzoine A Israelson N Keinan R Ben-Romano O Friedman V Shoshan-Barmatz 2009 The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins J Cell Sci 122 1906 1916 19461077 10.1242/jcs.040188 1:CAS:528:DC%2BD1MXosVCntLk%3D
2. U Ahting M Thieffry H Engelhardt R Hegerl W Neupert S Nussberger 2001 Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria J Cell Biol 153 1151 1160 11402060 10.1083/jcb.153.6.1151 1:CAS:528:DC%2BD3MXktlOmsLk%3D (Pubitemid 34289255)
3. T Arnold M Poynor S Nussberger AN Lupas D Linke 2007 Gene duplication of the eight-stranded β-barrel protein OmpX produces a functional pore: a scenario for the evolution of transmembrane β-barrels J Mol Biol 336 1174 1184 10.1016/j.jmb.2006.12.029 (Pubitemid 46186395)
4. M Bayrhuber T Meins M Habeck S Becker K Giller S Villinger C Vonrhein C Griesinger M Zweckstetter K Zeth 2008 Structure of the human voltage-dependent anion channel Proc Natl Acad Sci USA 105 15370 15375 18832158 10.1073/pnas.0808115105 1:CAS:528:DC%2BD1cXht1Gnt7%2FM
5. L Becker M Bannwarth C Meisinger K Hill K Model T Krimmer R Casadio KN Truscott GE Schulz N Pfanner R Wagner 2005 Preprotein translocase of the outer mitochondrial membrane: reconstituted Tom40 forms a characteristic TOM pore J Mol Biol 353 1011 1020 16213519 10.1016/j.jmb.2005.09.019 1:CAS:528: DC%2BD2MXhtFKms7jK (Pubitemid 41503269)
6. A Chacinska CM Koehler D Milenkovic T Lithgow N Pfanner 2009 Importing mitochondrial proteins: machineries and mechanisms Cell 138 628 644 19703392 10.1016/j.cell.2009.08.005 1:CAS:528:DC%2BD1MXhsVCjs73L
7. T Endo K Yamano 2009 Multiple pathways for mitochondrial protein traffic Biol Chem 390 723 730 19453276 10.1515/BC.2009.087 1:CAS:528: DC%2BD1MXps1ylsL0%3D
8. T Endo K Yamano S Kawano 2011 Structural insight into the mitochondrial protein import system Biochim Biophys Acta 1808 955 970 20655871 10.1016/j.bbamem.2010.07.018 1:CAS:528:DC%2BC3MXhvFentbk%3D
9. H Engelhardt T Meins M Poynor V Adams S Nussberger W Welte K Zeth 2007 High level expression, refolding and probing the natural fold of the human voltage-dependent anion channel isoforms I and II J Membr Biol 216 93 105 17828567 10.1007/s00232-007-9038-8 1:CAS:528:DC%2BD2sXhtVOkurvP (Pubitemid 47479553)
10. Fabian H, Schultz CP (2000) Fourier transform infrared spectroscopy in peptide and protein analysis. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, Chichester, pp 5779-5803
11. Fersht A (1999) Structure and mechanism in protein science: a guide to enzyme catalysis and protein folding. W.H. Freeman and Company, pp 1-631
12. Harsman A, Krüger V, Bartsch P, Honigmann A, Schmidt O, Rao S, Meisinger C, Wagner R (2010) Protein conducting nanopores. J Phys Condens Matter 22:454102
13. K Hill K Model MT Ryan K Dietmeier F Martin R Wagner N Pfanner 1998 Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins Nature 395 516 521 9774109 10.1038/26780 1:CAS:528:DyaK1cXms1aks78%3D (Pubitemid 28462448)
14. S Hiller RG Garces TJ Malia VY Orekhov M Colombini G Wagner 2008 Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321 1206 1210 18755977 10.1126/science.1161302 1:CAS:528: DC%2BD1cXhtVGgt7zI
15. AD Humphries IC Streimann D Stojanovski AJ Johnston M Yano NJ Hoogenraad MT Ryan 2005 Dissection of the mitochondrial import and assembly pathway for human Tom40 J Biol Chem 280 11535 11543 15644312 10.1074/jbc.M413816200 1:CAS:528:DC%2BD2MXisVyjtro%3D (Pubitemid 40418465)
16. DT Jones 1999 Protein secondary structure prediction based on position-specific scoring matrices J Mol Biol 292 195 202 10493868 10.1006/jmbi.1999.3091 1:CAS:528:DyaK1MXlvFyksb0%3D (Pubitemid 29435759)
17. J Kinoshita K Mihara T Oka 2007 Identification and characterization of a new Tom40 isoform, a central component of mitochondrial outer membrane translocase J Biochem 141 897 906 17437969 10.1093/jb/mvm097 1:CAS:528:DC%2BD2sXhtV2ntrjF (Pubitemid 351455330)
18. KP Künkele S Heins M Dembowski FE Nargang R Benz M Thieffry J Walz R Lill S Nussberger W Neupert 1998 The preprotein translocation channel of the outer membrane of mitochondria Cell 93 1009 1019 9635430 10.1016/S0092-8674(00) 81206-4 (Pubitemid 28280794)
19. D Macasev E Newbigin J Whelan T Lithgow 2000 How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts Plant Physiol 123 811 816 10889230 10.1104/pp.123.3.811 1:CAS:528:DC%2BD3cXlt1SlsLg%3D (Pubitemid 30466833)
20. D Macasev J Whelan E Newbigin MC Silva-Filho TD Mulhern T Lithgow 2004 Tom22′, an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes Mol Biol Evol 21 1557 1564 15155803 10.1093/molbev/msh166 1:CAS:528:DC%2BD2cXmtlKgt7s%3D (Pubitemid 38971766)
21. F Mager L Sokolova J Lintzel B Brutschy S Nussberger 2010 LILBID-mass spectrometry of the mitochondrial preprotein translocase TOM J Phys Condens Matter 22 454132 21339618 10.1088/0953-8984/22/45/454132
22. TJ Malia G Wagner 2007 NMR structural investigation of the mitochondrial outer membrane protein VDAC and its interaction with antiapoptotic Bcl-xL Biochemistry 46 514 525 17209561 10.1021/bi061577h 1:CAS:528:DC%2BD28Xht12iurzI (Pubitemid 46105440)
23. K Model T Prinz T Ruiz M Radermacher T Krimmer W Kühlbrandt N Pfanner C Meisinger 2002 Protein translocase of the outer mitochondrial membrane: role of import receptors in the structural organization of the TOM complex J Mol Biol 316 657 666 11866524 10.1006/jmbi.2001.5365 1:CAS:528:DC%2BD38XhsFSqtbg%3D (Pubitemid 34729247)
24. K Model C Meisinger W Kuhlbrandt 2008 Cryo-electron microscopy structure of a yeast mitochondrial preprotein translocase J Mol Biol 383 1049 1057 18706915 10.1016/j.jmb.2008.07.087 1:CAS:528:DC%2BD1cXht1KntrjI
25. D Mokranjac W Neupert 2009 Thirty years of protein translocation into mitochondria: unexpectedly complex and still puzzling Biochim Biophys Acta 1793 33 41 18672008 10.1016/j.bbamcr.2008.06.021 1:CAS:528:DC%2BD1cXhsVWrtL3L
26. Nussberger S, Neupert W (2002) Protein translocation across the outer membrane of mitochondria: structure and function of the TOM complex. In: Kasianowicz JJ, Kellermayer MSZ, Deamer DW (eds) Structure and dynamics of confined polymers. NATO science series. Kluwer Academic, Dordrecht, pp 67-84
27. CN Pace F Vajdos L Fee G Grimsley T Gray 1995 How to measure and predict the molar absorption coefficient of a protein Protein Sci 4 2411 2423 8563639 10.1002/pro.5560041120 1:CAS:528:DyaK2MXpsVGqt7k%3D
28. CN Pace EJ Hebert KL Shaw D Schell V Both D Krajcikova J Sevcik KS Wilson Z Dauter RW Hartley GR Grimsley 1998 Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2 and Sa3 J Mol Biol 279 271 286 9636716 10.1006/jmbi.1998.1760 1:CAS:528:DyaK1cXjvVOkt7c%3D (Pubitemid 28252145)
29. AJ Perry JM Hulett VA Likic T Lithgow PR Gooley 2006 Convergent evolution of receptors for protein import into mitochondria Curr Biol 16 221 229 16461275 10.1016/j.cub.2005.12.034 1:CAS:528:DC%2BD28XhtlKlt7w%3D (Pubitemid 43190221)
30. M Poynor R Eckert S Nussberger 2008 Dynamics of the preprotein translocation channel of the outer membrane of mitochondria Biophys J 95 1511 1522 18456827 10.1529/biophysj.108.131003 1:CAS:528:DC%2BD1cXovFWhurY%3D
31. H Prokisch S Nussberger B Westermann 2002 Protein import into mitochondria of Neurospora crassa Fungal Genet Biol 36 85 90 12081461 10.1016/S1087-1845(02)00018-X 1:CAS:528:DC%2BD38XkslKmu7s%3D (Pubitemid 34757033)
32. M Pusnik F Charriere P Maser RF Waller MJ Dagley T Lithgow A Schneider 2009 The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane Mol Biol Evol 26 671 680 19091722 10.1093/molbev/msn288 1:CAS:528:DC%2BD1MXhvF2ktr8%3D
33. ME Quinlan E Kerkhoff 2008 Actin nucleation: bacteria get in-Spired Nat Cell Biol 10 13 15 18172428 10.1038/ncb0108-13 1:CAS:528:DC%2BD1cXkvVek
34. M Romero-Ruiz KR Mahendran R Eckert M Winterhalter S Nussberger 2010 Interactions of mitochondrial presequence peptides with the mitochondrial outer membrane preprotein translocase TOM Biophys J 99 774 781 20682254 10.1016/j.bpj.2010.05.010 1:CAS:528:DC%2BC3cXpvFWnurw%3D
35. M Schwartz A Matouschek 1999 The dimensions of the protein import channels in the outer and inner mitochondrial membranes Proc Natl Acad Sci USA 9 13086 13090 10.1073/pnas.96.23.13086
36. N Sreerama RW Woody 2000 Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal Biochem 287 252 260 11112271 10.1006/abio.2000.4880 1:CAS:528:DC%2BD3cXosFGhu7Y%3D (Pubitemid 32006234)
37. N Sreerama RW Woody 2003 Structural composition of betaI- and betaII-proteins Protein Sci 12 384 388 12538903 10.1110/ps.0235003 1:CAS:528:DC%2BD3sXos1amsg%3D%3D (Pubitemid 36120352)
38. N Sreerama RW Woody 2004 Computation and analysis of protein circular dichroism spectra Methods Enzymol 383 318 351 15063656 10.1016/S0076-6879(04) 83013-1 1:CAS:528:DC%2BD2cXkt1Siu7o%3D (Pubitemid 38401795)
39. H Suzuki Y Okazawa T Komiya K Saeki E Mekada S Kitada A Ito K Mihara 2000 Characterization of Rat TOM40, a central component of the preprotein translocase of the mitochondrial outer membrane J Biol Chem 275 37930 37936 10980201 10.1074/jbc.M006558200 1:STN:280:DC%2BD3M%2FnvVeisQ%3D%3D (Pubitemid 32004913)
40. H Suzuki T Kadowaki M Maeda H Sasaki J Nabekura M Sakaguchi K Mihara 2004 Membrane-embedded C-terminal segment of rat mitochondrial TOM40 constitutes protein-conducting pore with enriched beta-structure J Biol Chem 279 50619 50629 15347672 10.1074/jbc.M408604200 1:CAS:528:DC%2BD2cXhtVWjsL%2FP (Pubitemid 39577879)
41. RD Taylor BJ McHale FE Nargang 2003 Characterization of Neurospora crassa Tom40-deficient mutants and effect of specific mutations on Tom40 assembly J Biol Chem 278 765 775 12399467 10.1074/jbc.M208083200 1:CAS:528:DC%2BD3sXnvVeq (Pubitemid 36790748)
42. R Ujwal D Cascio JP Colletier S Faham J Zhang L Toro P Ping J Abramson 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 18988731 10.1073/pnas.0809634105 1:CAS:528:DC%2BD1cXhsVCmur7P
43. W Werhahn A Niemeyer L Jansch VV Kruft UK Schmitz HP Braun 2001 Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20 Plant Physiol 125 943 954 11161051 10.1104/pp.125.2.943 1:CAS:528:DC%2BD3MXhs1Kltrk%3D (Pubitemid 32169901)
44. W Werhahn L Jänsch HP Braun 2003 Identification of novel subunits of the TOM complex of Arabidopsis thaliana Plant Physiol Biochem 41 407 416 10.1016/S0981-9428(03)00047-0 1:CAS:528:DC%2BD3sXktVyisro%3D (Pubitemid 36708596)
45. K Zeth 2010 Structure and evolution of mitochondrial outer membrane proteins of beta-barrel topology Biochim Biophys Acta 1797 1292 1299 20450883 10.1016/j.bbabio.2010.04.019 1:CAS:528:DC%2BC3cXnvV2qsr8%3D