Inserting membrane proteins: The YidC/Oxa1/Alb3 machinery in bacteria, mitochondria, and chloroplasts

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 3, 2011, Pages 866-875

  Wang, Peng ^a   Dalbey, Ross E ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN ALB3; PROTEIN OXA1; PROTEIN YIDC; SEC TRANSLOCASE; UNCLASSIFIED DRUG; YIDC2 PROTEIN;

AMINO TERMINAL SEQUENCE; BACTERIUM; BINDING AFFINITY; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CHLOROPLAST; EVOLUTIONARY HOMOLOGY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; THYLAKOID MEMBRANE;

BACTERIA; BACTERIAL PROTEINS; CHLOROPLASTS; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NUCLEAR PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 79851503908     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.08.014     Document Type: Review

References (120)

1. N. Altamura, N. Capitanio, N. Bonnefoy, S. Papa, and G. Dujardin The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase FEBS Lett 382 1996 111 115 (Pubitemid 26092240)
2. M. Bauer, M. Behrens, K. Esser, G. Michaelis, and E. Pratje PET1402, a nuclear gene required for proteolytic processing of cytochrome oxidase subunit 2 in yeast Mol Gen Genet 245 1994 272 278 (Pubitemid 24352412)
3. K. Beck, G. Eisner, D. Trescher, R.E. Dalbey, J. Brunner, and M. Muller YidC, an assembly site for polytopic Escherichia coli membrane proteins located in immediate proximity to the SecYE translocon and lipids EMBO Rep 2 2001 709 714 (Pubitemid 32798714)
4. G.R. Bender, S.V. Sutton, and R.E. Marquis Acid tolerance, proton permeabilities, and membrane ATPases of oral streptococci Infect Immun 53 1986 331 338 (Pubitemid 16073862)
5. M. Benz, T. Bals, I.L. Gugel, M. Piotrowski, A. Kuhn, D. Schunemann, J. Soll, and E. Ankele Alb4 of Arabidopsis promotes assembly and stabilization of a non chlorophyll-binding photosynthetic complex, the CF1CF0-ATP synthase Mol Plant 2 2009 1410 1424
6. N. Bonnefoy, F. Chalvet, P. Hamel, P.P. Slonimski, and G. Dujardin OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis J Mol Biol 239 1994 201 212 (Pubitemid 24210406)
7. N. Bonnefoy, H.L. Fiumera, G. Dujardin, and T.D. Fox Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes Biochim Biophys Acta 1793 2009 60 70
8. S.A. Broadley, C.M. Demlow, and T.D. Fox Peripheral mitochondrial inner membrane protein, Mss2p, required for export of the mitochondrially coded Cox2p C tail in Saccharomyces cerevisiae Mol Cell Biol 21 2001 7663 7672 (Pubitemid 32988777)
9. N. Celebi, L. Yi, S.J. Facey, A. Kuhn, and R.E. Dalbey Membrane biogenesis of subunit II of cytochrome bo oxidase: contrasting requirements for insertion of N-terminal and C-terminal domains J Mol Biol 357 2006 1428 1436
10. A. Chacinska, C.M. Koehler, D. Milenkovic, T. Lithgow, and N. Pfanner Importing mitochondrial proteins: machineries and mechanisms Cell 138 2009 628 644
11. M. Chen, J.C. Samuelson, F. Jiang, M. Muller, A. Kuhn, and R.E. Dalbey Direct interaction of YidC with the Sec-independent Pf3 coat protein during its membrane protein insertion J Biol Chem 277 2002 7670 7675 (Pubitemid 34968212)
12. K. Cline, and S.M. Theg The Sec and protein translocation pathways in chloroplast Ross E. Dalbey, Carla M. Koehler, Fuyuhiko Tamanoi, Molecular Machines Involved in Protein Transport across Cellular Membranes 3rd Edition The Enzymes Vol 25 2007 Academic Press San Diego 463 492
13. J. DeLille, E.C. Peterson, T. Johnson, M. Moore, A. Kight, and R. Henry A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts Proc Nat Acad Sci USA 97 2000 1926 1931 (Pubitemid 30118545)
14. Y. Dong, S.R. Palmer, A. Hasona, S. Nagamori, H.R. Kaback, R.E. Dalbey, and L.J. Brady Functional overlap but lack of complete cross-complementation of Streptococcus mutans and Escherichia coli YidC orthologs J Bacteriol 190 2008 2458 2469 (Pubitemid 351466341)
15. A.J. Driessen, and N. Nouwen Protein translocation across the bacterial cytoplasmic membrane Annu Rev Biochem 77 2008 643 667
16. D.J. du Plessis, N. Nouwen, and A.J. Driessen Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion J Biol Chem 281 2006 12248 12252 (Pubitemid 43855308)
17. S.J. Facey, S.A. Neugebauer, S. Krauss, and A. Kuhn The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli J Mol Biol 365 2007 995 1004 (Pubitemid 46014190)
18. Falk, S., S. Ravaud, J. Koch, and I. Sinning. The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J Biol Chem 285 (2010) 5954-5962.
19. S. Funes, F.E. Nargang, W. Neupert, and J.M. Herrmann The Oxa2 protein of Neurospora crassa plays a critical role in the biogenesis of cytochrome oxidase and defines a ubiquitous subbranch of the Oxa1/YidC/Alb3 protein family Mol Biol Cell 15 2004 1853 1861 (Pubitemid 38401833)
20. S. Funes, A. Hasona, H. Bauerschmitt, C. Grubbauer, F. Kauff, R. Collins, P.J. Crowley, S.R. Palmer, L.J. Brady, and J.M. Herrmann Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function Proc Natl Acad Sci USA 106 2009 6656 6661
21. M. Gaisne, and N. Bonnefoy The COX18 gene, involved in mitochondrial biogenesis, is functionally conserved and tightly regulated in humans and fission yeast FEMS Yeast Res 6 2006 869 882
22. I. Gentle, K. Gabriel, P. Beech, R. Waller, and T. Lithgow The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria J Cell Biol 164 2004 19 24 (Pubitemid 38082453)
23. L. Gerdes, T. Bals, E. Klostermann, M. Karl, K. Philippar, M. Hunken, J. Soll, and D. Schunemann A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana J Biol Chem 281 2006 16632 16642
24. B.S. Glick, and G. Von Heijne Saccharomyces cerevisiae mitochondria lack a bacterial-type sec machinery Protein Sci 5 1996 2651 2652 (Pubitemid 26424879)
25. B.S. Glick, E.M. Beasley, and G. Schatz Protein sorting in mitochondria Trends Biochem Sci 17 1992 453 459
26. V. Gohre, F. Ossenbuhl, M. Crevecoeur, L.A. Eichacker, and J.D. Rochaix One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas Plant Cell 18 2006 1454 1466 (Pubitemid 43956109)
27. M.R. Groves, A. Mant, A. Kuhn, J. Koch, S. Dubel, C. Robinson, and I. Sinning Functional characterization of recombinant chloroplast signal recognition particle J Biol Chem 276 2001 27778 27786
28. P. Hamel, C. Lemaire, N. Bonnefoy, P. Brivet-Chevillotte, and G. Dujardin Mutations in the membrane anchor of yeast cytochrome c1 compensate for the absence of Oxa1p and generate carbonate-extractable forms of cytochrome c1 Genetics 150 1998 601 611 (Pubitemid 28463039)
29. A. Hasona, P.J. Crowley, C.M. Levesque, R.W. Mair, D.G. Cvitkovitch, A.S. Bleiweis, and L.J. Brady Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2 Proc Natl Acad Sci USA 102 2005 17466 17471 (Pubitemid 41740889)
30. S. He, and T.D. Fox Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p Mol Biol Cell 8 1997 1449 1460 (Pubitemid 27385569)
31. S. He, and T.D. Fox Mutations affecting a yeast mitochondrial inner membrane protein, pnt1p, block export of a mitochondrially synthesized fusion protein from the matrix Mol Cell Biol 19 1999 6598 6607 (Pubitemid 29441844)
32. K. Hell, J. Herrmann, E. Pratje, W. Neupert, and R.A. Stuart Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space FEBS Lett 418 1997 367 370 (Pubitemid 27515959)
33. K. Hell, W. Neupert, and R.A. Stuart Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA EMBO J 20 2001 1281 1288 (Pubitemid 32233968)
34. R. Henry, R.L. Goforth, and D. Schunemann Chloroplast SRP/FtsY and Alb3 in protein integration into the thylakoid membrane Ross E. Dalbey, Carla M. Koehler, Fuyuhiko Tamanoi, Molecular Machines Involved in Protein Transport across Cellular Membranes 3rd Edition The Enzymes Vol 25 2007 Academic Press San Diego, CA 493 521
35. J.M. Herrmann, H. Koll, R.A. Cook, W. Neupert, and R.A. Stuart Topogenesis of cytochrome oxidase subunit II. Mechanisms of protein export from the mitochondrial matrix J Biol Chem 270 1995 27079 27086
36. J.M. Herrmann, W. Neupert, and R.A. Stuart Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p EMBO J 16 1997 2217 2226 (Pubitemid 27258625)
37. L. Jia, M. Dienhart, M. Schramp, M. McCauley, K. Hell, and R.A. Stuart Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1 EMBO J 22 2003 6438 6447 (Pubitemid 38009592)
38. L. Jia, M.K. Dienhart, and R.A. Stuart Oxa1 directly interacts with Atp9 and mediates its assembly into the mitochondrial F1Fo-ATP synthase complex Mol Biol Cell 18 2007 1897 1908 (Pubitemid 46717569)
39. F. Jiang, L. Yi, M. Moore, M. Chen, T. Rohl, K.J. Van Wijk, J.W. De Gier, R. Henry, and R.E. Dalbey Chloroplast YidC homolog Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins J Biol Chem 277 2002 19281 19288 (Pubitemid 34967432)
40. F. Jiang, M. Chen, L. Yi, J.W. de Gier, A. Kuhn, and R.E. Dalbey Defining the regions of Escherichia coli YidC that contribute to activity J Biol Chem 278 2003 48965 48972
41. S.E. Jones, L.J. Lloyd, K.K. Tan, and M. Buck Secretion defects that activate the phage shock response of Escherichia coli J Bacteriol 185 2003 6707 6711 (Pubitemid 37385892)
42. F. Kessler, and D. Schnell Chloroplast biogenesis: diversity and regulation of the protein import apparatus Curr Opin Cell Biol 21 2009 494 500
43. D. Kiefer, and A. Kuhn YidC as an essential and multifunctional component in membrane protein assembly Int Rev Cytol 259 2007 113 138 (Pubitemid 46529408)
44. C. Klenner, J. Yuan, R.E. Dalbey, and A. Kuhn The Pf3 coat protein contacts TM1 and TM3 of YidC during membrane biogenesis FEBS Lett 582 2008 3967 3972
45. E. Klostermann, I. Droste Gen Helling, J.P. Carde, and D. Schunemann The thylakoid membrane protein ALB3 associates with the cpSecY- translocase in Arabidopsis thaliana Biochem J 368 2002 777 781 (Pubitemid 36042679)
46. T.J. Knowles, A. Scott-Tucker, M. Overduin, and I.R. Henderson Membrane protein architects: the role of the BAM complex in outer membrane protein assembly Nat Rev Microbiol 7 2009 206 214
47. N. Kogata, K. Nishio, T. Hirohashi, S. Kikuchi, and M. Nakai Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids FEBS Lett 447 1999 329 333 (Pubitemid 29146112)
48. R. Kohler, D. Boehringer, B. Greber, R. Bingel-Erlenmeyer, I. Collinson, C. Schaffitzel, and N. Ban YidC and Oxa1 form dimeric insertion pores on the translating ribosome Mol Cell 34 2009 344 353
49. S. Kol, N. Nouwen, and A.J. Driessen Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes J Biol Chem 283 2008 31269 31273
50. V. Kozjak, N. Wiedemann, D. Milenkovic, C. Lohaus, H.E. Meyer, B. Guiard, C. Meisinger, and N. Pfanner An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane J Biol Chem 278 2003 48520 48523 (Pubitemid 41079488)
51. B.F. Lang, G. Burger, C.J. O'Kelly, R. Cedergren, G.B. Golding, C. Lemieux, D. Sankoff, M. Turmel, and M.W. Gray An ancestral mitochondrial DNA resembling a eubacterial genome in miniature Nature 387 1997 493 497 (Pubitemid 27235465)
52. C. Lemaire, P. Hamel, J. Velours, and G. Dujardin Absence of the mitochondrial AAA protease Yme1p restores F0-ATPase subunit accumulation in an oxa1 deletion mutant of Saccharomyces cerevisiae J Biol Chem 275 2000 23471 23475 (Pubitemid 30624627)
53. X. Li, R. Henry, J. Yuan, K. Cline, and N.E. Hoffman A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes Proc Natl Acad Sci USA 92 1995 3789 3793
54. J. Luirink, and I. Sinning SRP-mediated protein targeting: structure and function revisited Biochim Biophys Acta 1694 2004 17 35 (Pubitemid 39535059)
55. Mathieu, L., M. Bourens, S. Marsy, O. Hlavacek, C. Panozzo, and G. Dujardin. A mutational analysis reveals new functional interactions between domains of the Oxa1 protein in Saccharomyces cerevisiae. Mol Microbiol 75:474-88.
56. D. Milenkovic, V. Kozjak, N. Wiedemann, C. Lohaus, H.E. Meyer, B. Guiard, N. Pfanner, and C. Meisinger Sam35 of the mitochondrial protein sorting and assembly machinery is a peripheral outer membrane protein essential for cell viability J Biol Chem 279 2004 22781 22785 (Pubitemid 38679479)
57. M. Moore, M.S. Harrison, E.C. Peterson, and R. Henry Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes J Biol Chem 275 2000 1529 1532 (Pubitemid 30060764)
58. M. Moore, R.L. Goforth, H. Mori, and R. Henry Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required J Cell Biol 162 2003 1245 1254 (Pubitemid 37210881)
59. R.M. Mould, J.S. Knight, E. Bogsch, and J.C. Gray Azide-sensitive thylakoid membrane insertion of chimeric cytochrome f polypeptides imported by isolated pea chloroplasts Plant J 11 1997 1051 1058 (Pubitemid 27236430)
60. S. Nagamori, I.N. Smirnova, and H.R. Kaback Role of YidC in folding of polytopic membrane proteins J Cell Biol 165 2004 53 62 (Pubitemid 38649176)
61. F.E. Nargang, M. Preuss, W. Neupert, and J.M. Herrmann The Oxa1 protein forms a homooligomeric complex and is an essential part of the mitochondrial export translocase in Neurospora crassa J Biol Chem 277 2002 12846 12853 (Pubitemid 34952649)
62. R. Nilsson, J. Brunner, N.E. Hoffman, and K.J. van Wijk Interactions of ribosome nascent chain complexes of the chloroplast- encoded D1 thylakoid membrane protein with cpSRP54 EMBO J 18 1999 733 742 (Pubitemid 29057258)
63. N. Nouwen, and A.J. Driessen SecDFyajC forms a heterotetrameric complex with YidC Mol Microbiol 44 2002 1397 1405 (Pubitemid 34595769)
64. J. Nunnari, T.D. Fox, and P. Walter A mitochondrial protease with two catalytic subunits of nonoverlapping specificities Science 262 1993 1997 2004 (Pubitemid 24041877)
65. D.C. Oliver, and M. Paetzel Crystal structure of the major periplasmic domain of the bacterial membrane protein assembly facilitator YidC J Biol Chem 283 2008 5208 5216
66. F. Ossenbuhl, V. Gohre, J. Meurer, A. Krieger-Liszkay, J.D. Rochaix, and L.A. Eichacker Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3 Plant Cell 16 2004 1790 1800 (Pubitemid 38908776)
67. M. Ott, and J.M. Herrmann Co-translational membrane insertion of mitochondrially encoded proteins Biochim Biophys Acta 1803 2009 767 775
68. S.A. Paschen, T. Waizenegger, T. Stan, M. Preuss, M. Cyrklaff, K. Hell, D. Rapaport, and W. Neupert Evolutionary conservation of biogenesis of beta-barrel membrane proteins Nature 426 2003 862 866 (Pubitemid 38056874)
69. M. Pohlschroder, E. Hartmann, N.J. Hand, K. Dilks, and A. Haddad Diversity and evolution of protein translocation Annu Rev Microbiol 59 2005 91 111 (Pubitemid 41507425)
70. O.I. Pop, Z. Soprova, G. Koningstein, D.J. Scheffers, P. van Ulsen, D. Wickstrom, J.W. de Gier, and J. Luirink YidC is required for the assembly of the MscL homopentameric pore FEBS J 276 2009 4891 4899
71. M. Preuss, M. Ott, S. Funes, J. Luirink, and J.M. Herrmann Evolution of mitochondrial oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery J Biol Chem 280 2005 13004 13011
72. C.E. Price, and A.J. Driessen YidC is involved in the biogenesis of anaerobic respiratory complexes in the inner membrane of Escherichia coli J Biol Chem 283 2008 26921 26927
73. Price, C.E., and A.J. Driessen. Conserved negative charges in the transmembrane segments of subunit K of the NADH:ubiquinone oxidoreductase determine its dependence on YidC for membrane insertion. J Biol Chem 285 (2010) 3575-3581.
74. S. Ravaud, G. Stjepanovic, K. Wild, and I. Sinning The crystal structure of the periplasmic domain of the Escherichia coli membrane protein insertase YidC contains a substrate binding cleft J Biol Chem 283 2008 9350 9358
75. A. Saaf, M. Monne, J.W. de Gier, and G. von Heijne Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli J Biol Chem 273 1998 30415 30418 (Pubitemid 28545514)
76. M.J. Saller, F. Fusetti, and A.J. Driessen Bacillus subtilis SpoIIIJ and YqjG function in membrane protein biogenesis J Bacteriol 191 2009 6749 6757
77. J.C. Samuelson, M. Chen, F. Jiang, I. Moller, M. Wiedmann, A. Kuhn, G.J. Phillips, and R.E. Dalbey YidC mediates membrane protein insertion in bacteria Nature 406 2000 637 641 (Pubitemid 30641051)
78. J.C. Samuelson, F. Jiang, L. Yi, M. Chen, J.W. de Gier, A. Kuhn, and R.E. Dalbey Function of YidC for the insertion of M13 procoat protein in E. coli: translocation of mutants that show differences in their membrane potential dependence and Sec- requirement J Biol Chem 16 2001 34847 34852
79. S.A. Saracco, and T.D. Fox Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane Mol Biol Cell 13 2002 1122 1131 (Pubitemid 34309610)
80. T. Sato, and K. Mihara Topogenesis of mammalian Oxa1, a component of the mitochondrial inner membrane protein export machinery J Biol Chem 284 2009 14819 14827
81. D. Schuenemann, S. Gupta, F. Persello-Cartieaux, V.V. Klimyuk, J.D.G. Jones, L. Nussaume, and N.E. Hoffman A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes Proc Natl Acad Sci USA 95 1998 10312 10316 (Pubitemid 28415338)
82. R.M. Schwartz, and M.O. Dayhoff Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts Science 199 1978 395 403
83. P.A. Scotti, M.L. Urbanus, J. Brunner, J.W. de Gier, G. von Heijne, C. van der Does, A.J. Driessen, B. Oudega, and J. Luirink YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase EMBO J 19 2000 542 549 (Pubitemid 30093727)
84. J. Serek, G. Bauer-Manz, G. Struhalla, L. Van Den Berg, D. Kiefer, R. Dalbey, and A. Kuhn Escherichia coli YidC is a membrane insertase for Sec-independent proteins EMBO J 23 2004 294 301 (Pubitemid 38294494)
85. J.G. Sklar, T. Wu, L.S. Gronenberg, J.C. Malinverni, D. Kahne, and T.J. Silhavy Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli Proc Natl Acad Sci USA 104 2007 6400 6405 (Pubitemid 47186106)
86. R.L. Souza, N.S. Green-Willms, T.D. Fox, A. Tzagoloff, and F.G. Nobrega Cloning and characterization of COX18, a Saccharomyces cerevisiae PET gene required for the assembly of cytochrome oxidase J Biol Chem 275 2000 14898 14902 (Pubitemid 30337204)
87. K.F. Stengel, I. Holdermann, P. Cain, C. Robinson, K. Wild, and I. Sinning Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43 Science 321 2008 253 256 (Pubitemid 351989097)
88. L. Stiburek, D. Fornuskova, L. Wenchich, M. Pejznochova, H. Hansikova, and J. Zeman Knockdown of human Oxa1l impairs the biogenesis of F1Fo-ATP synthase and NADH:ubiquinone oxidoreductase J Mol Biol 374 2007 506 516 (Pubitemid 350007656)
89. R.A. Stuart, and W. Neupert Making membranes in bacteria [comment] [news] Nature 406 2000 575 577 (Pubitemid 30641029)
90. E. Sundberg, J.G. Slagter, I. Fridborg, S.P. Cleary, C. Robinson, and G. Coupland ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria Plant Cell 9 1997 717 730 (Pubitemid 28104502)
91. G. Szyrach, M. Ott, N. Bonnefoy, W. Neupert, and J.M. Herrmann Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria EMBO J 22 2003 6448 6457 (Pubitemid 38009593)
92. H. Tjalsma, S. Bron, and J.M. van Dijl Complementary impact of paralogous Oxa1-like proteins of Bacillus subtilis on post-translocational stages in protein secretion J Biol Chem 278 2003 15622 15632 (Pubitemid 36799672)
93. H. Tokuda, and S. Matsuyama Sorting of lipoproteins to the outer membrane in E. coli Biochim Biophys Acta 1694 2004 IN1 IN9
94. C.J. Tu, D. Schuenemann, and N.E. Hoffman Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes J Biol Chem 274 1999 27219 27224
95. C.J. Tu, E.C. Peterson, R. Henry, and N.E. Hoffman The L18 domain of light-harvesting chlorophyll proteins binds to chloroplast signal recognition particle 43 J Biol Chem 275 2000 13187 13190 (Pubitemid 30257371)
96. N.D. Ulbrandt, J.A. Newitt, and H.D. Bernstein The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins Cell 88 1997 187 196 (Pubitemid 28015867)
97. M.L. Urbanus, P.A. Scotti, L. Froderberg, A. Saaf, J.W. de Gier, J. Brunner, J.C. Samuelson, R.E. Dalbey, B. Oudega, and J. Luirink Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC EMBO Rep 2 2001 524 529 (Pubitemid 32611350)
98. M.L. Urbanus, L. Froderberg, D. Drew, P. Bjork, J.W. de Gier, J. Brunner, B. Oudega, and J. Luirink Targeting, insertion, and localization of Escherichia coli YidC J Biol Chem 277 2002 12718 12723 (Pubitemid 34952632)
99. E. van Bloois, G. Jan Haan, J.W. de Gier, B. Oudega, and J. Luirink F(1)F(0) ATP synthase subunit c is targeted by the SRP to YidC in the E. coli inner membrane FEBS Lett 576 2004 97 100 (Pubitemid 39330464)
100. E. van Bloois, S. Nagamori, G. Koningstein, R.S. Ullers, M. Preuss, B. Oudega, N. Harms, H.R. Kaback, J.M. Herrmann, and J. Luirink The Sec-independent function of Escherichia coli YidC is evolutionary-conserved and essential J Biol Chem 280 2005 12996 13003
101. E. van Bloois, G.J. Haan, J.W. de Gier, B. Oudega, and J. Luirink Distinct requirements for translocation of the N-tail and C-tail of the Escherichia coli inner membrane protein CyoA J Biol Chem 281 2006 10002 10009 (Pubitemid 43864533)
102. M. Van Der Laan, M.L. Urbanus, C.M. Ten Hagen-Jongman, N. Nouwen, B. Oudega, N. Harms, A.J. Driessen, and J. Luirink A conserved function of YidC in the biogenesis of respiratory chain complexes Proc Natl Acad Sci USA 100 2003 5801 5806 (Pubitemid 36576888)
103. M. Van Der Laan, P. Bechtluft, S. Kol, N. Nouwen, and A.J. Driessen F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis J Cell Biol 165 2004 213 222 (Pubitemid 38544524)
104. M. van der Laan, N. Nouwen, and A.J. Driessen SecYEG proteoliposomes catalyze the Deltaphi-dependent membrane insertion of FtsQ J Biol Chem 279 2004 1659 1664 (Pubitemid 38084432)
105. S. Wagner, O. Pop, G.J. Haan, L. Baars, G. Koningstein, M.M. Klepsch, P. Genevaux, J. Luirink, and J.W. de Gier Biogenesis of MalF and the MalFGK(2) maltose transport complex in Escherichia coli requires YidC J Biol Chem 283 2008 17881 17890
106. T. Waizenegger, S.J. Habib, M. Lech, D. Mokranjac, S.A. Paschen, K. Hell, W. Neupert, and D. Rapaport Tob38, a novel essential component in the biogenesis of beta-barrel proteins of mitochondria EMBO Rep 5 2004 704 709 (Pubitemid 39173006)
107. D.M. Walther, D. Rapaport, and J. Tommassen Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence Cell Mol Life Sci 66 2009 2789 2804
108. Wang, P., A. Kuhn, and R. E. Dalbey. Global change of gene expression and cell physiology in YidC-depleted E. coli. J Bacteriol 192 (2010) 2193-2209.
109. L. Weiner, and P. Model Role of an Escherichia coli stress-response operon in stationary-phase survival Proc Natl Acad Sci USA 91 1994 2191 2195 (Pubitemid 24092069)
110. C.A. Woolhead, S.J. Thompson, M. Moore, C. Tissier, A. Mant, A. Rodger, R. Henry, and C. Robinson Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion J Biol Chem 276 2001 40841 40846
111. T. Wu, J. Malinverni, N. Ruiz, S. Kim, T.J. Silhavy, and D. Kahne Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli Cell 121 2005 235 245 (Pubitemid 40546391)
112. K. Xie, and R.E. Dalbey Inserting proteins into the bacterial cytoplasmic membrane using the Sec and YidC translocases Nat Rev Microbiol 6 2008 234 244 (Pubitemid 351256318)
113. K. Xie, D. Kiefer, G. Nagler, R.E. Dalbey, and A. Kuhn Different regions of the nonconserved large periplasmic domain of Escherichia coli YidC are involved in the SecF interaction and membrane insertase activity Biochemistry 45 2006 13401 13408 (Pubitemid 44707701)
114. M.R. Yen, K.T. Harley, Y.H. Tseng, and M.H. Saier Jr. Phylogenetic and structural analyses of the oxa1 family of protein translocases FEMS Microbiol Lett 204 2001 223 231 (Pubitemid 33145258)
115. L. Yi, F. Jiang, M. Chen, B. Cain, A. Bolhuis, and R.E. Dalbey YidC is strictly required for membrane insertion of subunits a and c of the F(1)F(0)ATP synthase and SecE of the SecYEG translocase Biochemistry 42 2003 10537 10544 (Pubitemid 37071454)
116. L. Yi, N. Celebi, M. Chen, and R.E. Dalbey Sec/SRP requirements and energetics of membrane insertion of subunits a, b, and c of the Escherichia coli F1F0 ATP synthase J Biol Chem 279 2004 39260 39267 (Pubitemid 39258187)
117. Z. Yu, G. Koningstein, A. Pop, and J. Luirink The conserved third transmembrane segment of YidC contacts nascent Escherichia coli inner membrane proteins J Biol Chem 283 2008 34635 34642
118. J. Yuan, J.C. Zweers, J.M. van Dijl, and R.E. Dalbey Protein transport across and into cell membranes in bacteria and archaea Cell Mol Life Sci 67 2010 179 199
119. J. Yuan, G.J. Phillips, and R.E. Dalbey Isolation of cold-sensitive yidC mutants provides insights into the substrate profile of the YidC insertase and the importance of transmembrane 3 in YidC function J Bacteriol 189 2007 8961 8972
120. L. Zhang, V. Paakkarinen, M. Suorsa, and E.M. Aro A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis J Biol Chem 276 2010 37809 37814