From the Sec complex to the membrane insertase YidC

Biological Chemistry

Volumn 390, Issue 8, 2009, Pages 701-706

  Kuhn, Andreas ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Evolution of protein translocation; Membrane insertase; Membrane targeting; Sec translocase; Signal peptides; Signal recognition particle

Indexed keywords

AQUAPORIN 4; MEMBRANE PROTEIN; PROTEIN SECA; SECY PROTEIN; SECYEG PROTEIN; UNCLASSIFIED DRUG; YIDC PROTEIN;

CELL MEMBRANE; CELL TRANSPORT; CYTOPLASM; ENDOPLASMIC RETICULUM; EUKARYOTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SHORT SURVEY;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT; SIGNAL RECOGNITION PARTICLE;

EID: 70349459701     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.059     Document Type: Short Survey

References (50)

1. Beck, K., Eisner, G., Trescher, D., Dalbey, R.E., Brunner, J., and Müller, M. (2001). YidC, an assembly site for polytopic E. coli membrane proteins located in immediate proximity to the SecYE translocon and lipids. EMBO Rep. 2, 709-714.
2. Celebi, N., Yi, L., Facey, S., Kuhn, A., and Dalbey, R.E. (2006). Membrane biogenesis of subunit II of cytochrome bo oxidase: contrasting requirements for insertion of N-terminal and C-terminal domains. J. Mol. Biol. 357, 1428-1436.
3. Chen, M., Yuan, Y., Yi, L., Xie, K., Facey, S., Pradel, N., Wu, L.-F., Kuhn, A., and Dalbey, R.E. (2005). Involvement of SecDF and YidC in the membrane insertion of M13 procoat mutants. Biochemistry 44, 10741-10749.
4. Dalbey, R.E. and Kuhn, A. (2004). YidC family members are involved in the membrane insertion, lateral integration, folding, and assembly of membrane proteins. J. Cell Biol. 166, 769-774.
5. Driessen, A.J. and Nouwen, N. (2008). Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77, 643-667.
6. Duong, F. and Wickner, W.T. (1997). The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. 16, 4871-4879.
7. Funes, S., Nargang, F.E., Neupert, W., and Herrmann, J.M. (2004). 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, 1853-1861.
8. Gelis, I., Bonvin, A.M., Keramisanou, D., Koukaki, M., Gouridis, G., Karamanou, S., Economou, A., and Kalodimos, C.G. (2007). Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131, 756-769.
9. Gerdes, L., Bals, T., Klostermann, E., Karl, M., Philippar, K., Hünken, M., Soll, J., and Schünemann, D. (2006). A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J. Biol. Chem. 281, 16632-16642.
10. Gerken, U., Erhardt, D., Schubert, A., Bä r, G., Ghosh, R., and Kuhn, A. (2008). Initial binding process of the membrane insertase YidC with its substrate protein Pf3 coat. Biochemistry 47, 6052-6058.
11. Halic, M., Blau, M., Becker, T., Mielke, T., Pool, M.R., Wild, K., Sinning, I., and Beckmann, R. (2006). Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 444, 507-511.
12. Hasona, A., Crowley, P.J., Levesque, C.M., Mair, R.W., Cvitkovitch, D.G., Bleiweis, A.S., and Brady, L.J. (2005). Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. Proc. Natl. Acad. Sci. USA 102, 17466-17471.
13. He, S. and Fox, T.D. (1997). 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, 1449-1460.
14. Hell, K., Neupert, W., and Stuart, R.A. (2001). Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20, 1281-1288.
15. Jia, L., Dienhart, M.K., and Stuart, R.A. (2007). Oxa1 directly interacts with Atp9 and mediates its assembly into the mitochondrial F1Fo-ATP synthase complex. Mol. Biol. Cell 18, 1897-1908.
16. Jiang, F., Yi, L., Moore, M., Chen, M., Rohl, T., van Wijk, K.J., de Gier, J.W., Henry, R., and Dalbey, R.E. (2002). 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, 19281-19288.
17. Jiang, F., Chen, M., Yi, L., de Gier, J.W., Kuhn, A., and Dalbey, R.E. (2003). Defining the regions of Escherichia coli YidC that contribute to activity. J. Biol. Chem. 278, 48965-48972.
18. Karamanou, S., Bariami, V., Papanikou, E., Kalodimos, C.G., and Economou, A. (2008). Assembly of the translocase motor onto the preprotein-conducting channel. Mol. Mircobiol. 70, 311-322.
19. Keenan, R.J., Freymann, D.M., Stroud, R.M., and Walter, P. (2001). The signal recognition particle. Annu. Rev. Biochem. 70, 755-775.
20. Klenner, C., Yuan, J., Dalbey, R.E., and Kuhn, A. (2008). The Pf3 coat protein contacts TM1 and TM3 of YidC during membrane biogenesis. FEBS Lett. 582, 3967-3972.
21. Kol, S., Nouwen, N., and Driessen, A.J. (2008). Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes. J. Biol. Chem. 283, 31269-31273.
22. Kuhn, A., Kiefer, D., Kö hne, C., Zhu, H.-Y., Tschantz, W., and Dalbey, R.E. (1994). Evidence for a loop-like insertion mechanism of pro-OmpA into the inner membrane of Escherichia coli. Eur. J. Biochem. 226, 891-897.
23. Kuhn, A., Stuart, R., Henry, R., and Dalbey, R. (2003). A new family of proteins catalyzes the membrane insertion process of proteins. Trends Cell Biol. 13, 510-516.
24. Li, W., Schulman, S., Boyd, D., Erlandson, K., Beckwith, J., and Rapoport, T.A. (2007). The plug domain of the SecY protein stabilizes the closed state of the translocation channel and maintains a membrane seal. Mol. Cell 26, 459-460.
25. Luirink, J. and Sinning, I. (2004). SRP-mediated protein targeting: structure and function revisited. Biochem. Biophys. Acta 1694, 17-35.
26. Maier, K., Hubich, S., Liebhart, H., Krauss, S., Kuhn, A., and Facey, S. (2008). An amphiphilic region in the cytoplasmic domain of KdpD is recognized by SRP and targeted to the E. coli membrane. Mol. Microbiol. 68,1471-1484.
27. Moore, M., Harrison, M.S., Peterson, E.C., and Henry, R. (2000). Chloroplast Oxa1p homolog albino3 is required for posttranslational integration of the light harvesting chlorophyllbinding protein into thylakoid membranes. J. Biol. Chem. 275, 1529-1532.
28. Nouwen, N. and Driessen, A.J. (2002). SecDFyajC forms a heterotetrameric complex with YidC. Mol. Microbiol. 44, 1397-1405.
29. Papanikou, E., Karamanou, S., Baud, C., Frank, M., Sianidis, G., Keramissanou, D., Kalodimos, C., Kuhn, A., and Economou, A. (2005). Identification of the preprotein binding domain of SecA. J. Biol. Chem. 280, 43209-43217.
30. Papanikou, E., Karamanou, S., and Economou, A. (2007). Bacterial protein secretion through the translocase nanomachine. Nat. Rev. Microbiol. 5, 839-851.
31. Perry, A.J., Rimmer, K.A., Mertens, H.D., Waller, R.F., Mulhern, T.D., Lithgow, T., and Gooley, P.R. (2008). Structure, topology and function of the translocase of the outer membrane of mitochondria. Plant Physiol. Biochem. 46, 265-274.
32. Plath, K., Mothes, W., Wilkinson, B.M., Stirling, C.J., and Rapoport, T.A. (1998). Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807.
33. Pogliano, J.A. and Beckwith, J. (1994). SecD and SecF facilitate protein export in Escherichia coli. EMBO J. 13, 554-561.
34. Preuss, M., Ott, M., Funes, S., Luirink, J., and Herrmann, J.M. (2005). Evolution of mitochondrial oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J. Biol. Chem. 280, 13004-13011.
35. Randall, L.L., Crane, J.M., Liu, G., and Hardy, S.J. (2004). Sites of interaction between SecA and the chaperone SecB, two proteins involved in export. Protein Sci. 13, 1124-1133.
36. Ravaud, S., Stjepanovic, G., Wild, K., and Sinning, I. (2008). The crystal structure of the periplasmic domain of the E. coli membrane protein insertase YidC contains a substrate binding cleft. J. Biol. Chem. 283, 9350-9358.
37. Sadlish, H., Pitonzo, D., Johnson, A.E., and Skach, W.R. (2005). Sequential triage of transmembrane segments by Sec61a during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 12, 870-878.
38. Samuelson, J.C., Jiang, F., Yi, L., Chen, M., Kuhn A., and Dalbey, R.E. (2001). 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 Secrequirement. J. Biol. Chem. 276, 34847-34852.
39. Sauri, A., McCormick, P.J., Johnson, A.E., and Mingarro, I. (2007). Sec61a and TRAM are sequentially adjacent to a nascent viral membrane protein during its ER integration. J. Mol. Biol. 366, 366-374.
40. Serek, J., Bauer-Manz, G., Struhalla, G., Vandenberg, L., Kiefer, D., Dalbey, R.E., and Kuhn, A. (2004). Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J. 23, 294-301.
41. Tö rnroth-Horsefield, S., Gourdon, P., Horsefield, R., Brive, L., Yamamoto, N., Mori, H., Snijder, A., and Neutze, R. (2007). Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 15, 1663-1673.
42. Urbanus, M.L., Scotti, P.A., Frö derberg, L., Sä ä f, A., de Gier, J.W.L., Brunner, J., Samuelson, J.C., Dalbey, R.E., Oudega, B., and Luirink, J. (2001). Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep. 2, 524-529.
43. van Bloois, E., Koningstein, G., Bauerschmitt, H., Herrmann, J.M., and Luirink, J. (2007). Saccharomyces cerevisiae Cox18 complements the essential Sec-independent function of E. coli YidC. FEBS Lett. 274, 5704-5713.
44. van den Berg, B., Clemons, W.M. Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S.C., and Rapoport, T.A. (2004). X-ray structure of a protein-conducting channel. Nature 427, 36-44.
45. Vrontou, E. and Economou, A. (2004). Structure and function of SecA, the preprotein translocase nanomotor. Biochem. Biophys. Acta 1694, 67-80.
46. Yen, M.R., Harley, K.T., Tseng, Y.H., and Saier, M.H. Jr. (2001). Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol. Lett. 204, 223-231.
47. Yu, Z., Koningstein, G., Pop, A., and Luirink, J. (2008). The conserved third transmembrane segment of YidC contacts nascent Escherichia coli inner membrane proteins. J. Biol. Chem. 283, 34635-34642.
48. Yuan, J., Phillips, G.J., and Dalbey, R.E. (2007). Isolation of coldsensitive yidC mutants provides insights into the substrate profile of the YidC insertase and the importance of transmembrane 3 in YidC function. J. Bacteriol. 189, 8961-8972.
49. Xie, K., Kiefer, D., Nagler, G., Dalbey, R.E., and Kuhn, A. (2006). Different regions of the nonconserved large periplasmic domain of E. coli YidC are involved in the SecF interaction and membrane insertase activity. Biochemistry 45, 13401-13408.
50. Zimmer, J., Nam, Y., and Rapoport, T.A. (2008). Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455, 936-943.