Membrane protein insertion and assembly by the bacterial holo-Translocon SecYEG-SecDF-YajC-YidC

Biochemical Journal

Volumn 473, Issue 19, 2016, Pages 3341-32354

  Komar, Joanna ^a   Alvira, Sara ^a   Schulze, Ryan J ^a   Martin, Remy ^a   Nijeholt, Jelger A Lycklama ^b   Lee, Sarah C ^c   Dafforn, Tim R ^c   Deckers Hebestreit, Gabriele ^d   Berger, Imre ^a,b   Schaffitzel, Christiane ^a,b   Collinson, Ian ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; TRANSLOCON; ESCHERICHIA COLI PROTEIN;

ARTICLE; BILAYER MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; INNER MEMBRANE; MEMBRANE; NONHUMAN; PRIORITY JOURNAL; METABOLISM; PROCEDURES; SPECTROFLUOROMETRY;

BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; SPECTROMETRY, FLUORESCENCE;

EID: 85009952069     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160545     Document Type: Article

References (65)

1. van den Berg, B., Clemons, W.M., Collinson, I., Modis, Y., Hartmann, E., Harrison, S.C. et al. (2004) X-ray structure of a protein-conducting channel. Nature 427, 36-44 doi:10.1038/nature02218.
2. Hizlan, D., Robson, A., Whitehouse, S., Gold, V.A., Vonck, J., Mills, D. et al. (2012) Structure of the SecY complex unlocked by a preprotein mimic. Cell Rep. 1, 21-28 doi:10.1016/j.celrep.2011.11.003.
3. Corey, R.A., Allen, W.J., Komar, J., Masiulis, S., Menzies, S., Robson, A. et al. (2016) Unlocking the bacterial SecY translocon. Structure 24, 518-527 doi:10.1016/j.str.2016.02.001.
4. 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 doi:10.1038/nature07335.
5. Bischoff, L., Wickles, S., Berninghausen, O., van der Sluis, E.O. and Beckmann, R. (2014) Visualization of a polytopic membrane protein during SecY-mediated membrane insertion. Nat. Commun. 5, 4103 doi:10.1038/ncomms5103.
6. Brundage, L., Hendrick, J.P., Schiebel, E., Driessen, A.J. and Wickner, W. (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62, 649-657 doi:10.1016/0092-8674(90)90111-Q.
7. Collinson, I., Corey, R.A. and Allen, W.J. (2015) Channel crossing: how are proteins shipped across the bacterial plasma membrane? Philos. Trans. R. Soc. B 370 doi:10.1098/rstb.2015.0025.
8. Allen, W.J., Corey, R.A., Oatley, P., Sessions, R.B., Baldwin, S.A., Radford, S.E. et al. (2016) Two-way communication between SecY and SecA suggests a Brownian ratchet mechanism for protein translocation. eLife 5, e15598 doi:10.7554/eLife.15598.
9. Schulze, R.J., Komar, J., Botte, M., Allen, W.J., Whitehouse, S., Gold, V.A.M. et al. (2014) Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. Proc. Natl Acad. Sci. USA 111, 4844-4849 doi:10.1073/pnas.1315901111.
10. Müller, M., Koch, H.-G., Beck, K. and Schafer, U. (2001) Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 66, 107-157 doi:10.1016/S0079-6603(00)66028-2.
11. Poritz, M.A., Bernstein, H.D., Strub, K., Zopf, D., Wilhelm, H. and Walter, P. (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250, 1111-1117 doi:10.1126/science.1701272.
12. Ulbrandt, N.D., Newitt, J.A. and Bernstein, H.D. (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88, 187-196 doi:10.1016/S0092-8674(00)81839-5.
13. Geller, B.L. and Wickner, W. (1985) M13 procoat inserts into liposomes in the absence of other membrane proteins. J. Biol. Chem. 260, 13281-13285 PMID: 3902814.
14. Kiefer, D. and Kuhn, A. (1999) Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. EMBO J. 18, 6299-6306 doi:10.1093/emboj/18.22.6299.
15. Samuelson, J.C., Chen, M., Jiang, F., Möller, I., Wiedmann, M., Kuhn, A. et al. (2000) Yidc mediates membrane protein insertion in bacteria. Nature 406, 637-641 doi:10.1038/35020586.
16. Wolfe, P.B., Rice, M. and Wickner, W. (1985) Effects of two sec genes on protein assembly into the plasma membrane of Escherichia coli. J. Biol. Chem. 260, 1836-1841 PMID: 3881443.
17. Yi, L., Celebi, N., Chen, M. and Dalbey, R.E. (2004) 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, 39260-39267 doi:10.1074/jbc.M405490200.
18. van der Laan, M., Bechtluft, P., Kol, S., Nouwen, N. and Driessen, A.J.M. (2004) F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J. Cell Biol. 165, 213-222 doi:10.1083/jcb.200402100.
19. Facey, S.J., Neugebauer, S.A., Krauss, S. and Kuhn, A. (2007) The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli. J. Mol. Biol. 365, 995-1004 doi:10.1016/j.jmb.2006.10.083.
20. Houben, E.N.G., Scotti, P.A., Valent, Q.A., Brunner, J., de Gier, J.-W.L., Oudega, B. et al. (2000) Nascent Lep inserts into the Escherichia coli inner membrane in the vicinity of YidC, SecY and SecA. FEBS Lett. 476, 229-233 doi:10.1016/S0014-5793(00)01735-X.
21. van der Laan, M., Houben, E.N.G., Nouwen, N., Luirink, J. and Driessen, A.J.M. (2001) Reconstitution of Sec-dependent membrane protein insertion: nascent FtsQ interacts with YidC in a SecYEG-dependent manner. EMBO Rep. 2, 519-523 doi:10.1093/embo-reports/kve106.
22. Urbanus, M.L., Scotti, P.A., Froderberg, L., Saaf, A., de Gier, J.-W.L., Brunner, J. et al. (2001) Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep. 2, 524-529 doi:10.1093/embo-reports/kve108.
23. Celebi, N., Yi, L., Facey, S.J., 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 doi:10.1016/j.jmb.2006.01.030.
24. Kol, S., Majczak, W., Heerlien, R., van der Berg, J.P., Nouwen, N. and Driessen, A.J.M. (2009) Subunit a of the F1F0 ATP synthase requires YidC and SecYEG for membrane insertion. J. Mol. Biol. 390, 893-901 doi:10.1016/j.jmb.2009.05.074.
25. Sachelaru, I., Petriman, N.A., Kudva, R., Kuhn, P., Welte, T., Knapp, B. et al. (2013) YidC occupies the lateral gate of the SecYEG translocon and is sequentially displaced by a nascent membrane protein. J. Biol. Chem. 288, 16295-16307 doi:10.1074/jbc.M112.446583.
26. Kumazaki, K., Kishimoto, T., Furukawa, A., Mori, H., Tanaka, Y., Dohmae, N. et al. (2014) Crystal structure of Escherichia coli YidC, a membrane protein chaperone and insertase. Sci. Rep. 4, 7299 doi:10.1038/srep07299.
27. Kumazaki, K., Chiba, S., Takemoto, M., Furukawa, A., Nishiyama, K.-i., Sugano, Y. et al. (2014) Structural basis of Sec-independent membrane protein insertion by YidC. Nature 509, 516-520 doi:10.1038/nature13167.
28. Ulmschneider, M.B., Ulmschneider, J.P., Schiller, N., Wallace, B.A., von Heijne, G. and White, S.H. (2014) Spontaneous transmembrane helix insertion thermodynamically mimics translocon-guided insertion. Nat. Commun. 5, 4863 doi:10.1038/ncomms5863.
29. Arechaga, I., Butler, P.J.G. and Walker, J.E. (2002) Self-assembly of ATP synthase subunit c rings. FEBS Lett. 515, 189-193 doi:10.1016/S0014-5793(02)02447-X.
30. Collinson, I., Breyton, C., Duong, F., Tziatzios, C., Schubert, D., Or, E. et al. (2001) Projection structure and oligomeric properties of a bacterial core protein translocase. EMBO J. 20, 2462-2471 doi:10.1093/emboj/20.10.2462.
31. Lotz, M., Haase, W., Kühlbrandt, W. and Collinson, I. (2008) Projection structure of yidC: a conserved mediator of membrane protein assembly. J. Mol. Biol. 375, 901-907 doi:10.1016/j.jmb.2007.10.089.
32. Ballhausen, B., Altendorf, K. and Deckers-Hebestreit, G. (2009) Constant c10 ring stoichiometry in the Escherichia coli ATP synthase analyzed by cross-linking. J. Bacteriol. 191, 2400-2404 doi:10.1128/JB.01390-08.
33. Bieniossek, C., Nie, Y., Frey, D., Olieric, N., Schaffitzel, C., Collinson, I. et al. (2009) Automated unrestricted multigene recombineering for multiprotein complex production. Nat. Methods 6, 447-450 doi:10.1038/nmeth.1326.
34. Deville, K., Gold, V.A.M., Robson, A., Whitehouse, S., Sessions, R.B., Baldwin, S.A. et al. (2011) The oligomeric state and arrangement of the active bacterial translocon. J. Biol. Chem. 286, 4659-4669 doi:10.1074/jbc.M110.175638.
35. Breyton, C., Haase, W., Rapoport, T.A., Kühlbrandt, W. and Collinson, I. (2002) Three-dimensional structure of the bacterial protein-translocation complex SecYEG. Nature 418, 662-665 doi:10.1038/nature00827.
36. Birkenhäger, R., Greie, J.-C., Altendorf, K. and Deckers-Hebestreit, G. (1999) F0 complex of the Escherichia coli ATP synthase. Not all monomers of the subunit c oligomer are involved in F1 interaction. Eur. J. Biochem. 264, 385-396 doi:10.1046/j.1432-1327.1999.00652.x.
37. Lee, S.C., Knowles, T.J., Postis, V.L.G., Jamshad, M., Parslow, R.A., Lin, Y.-P. et al. (2016) A method for detergent-free isolation of membrane protein with its local lipid environment. Nat. Protoc. doi:10.1038/nprot.2016.070.
38. Robson, A., Gold, V.A.M., Hodson, S., Clarke, A.R. and Collinson, I. (2009) Energy transduction in protein transport and the ATP hydrolytic cycle of SecA. Proc. Natl Acad. Sci. USA 106, 5111-5116 doi:10.1073/pnas.0809592106.
39. Oesterhelt, D. and Stoeckenius, W. (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31, 667-678 doi:10.1016/0076-6879(74)31072-5.
40. Schaffitzel, C. and Ban, N. (2007) Generation of ribosome nascent chain complexes for structural and functional studies. J. Struct. Biol. 158, 463-471 doi:10.1016/j.jsb.2007.01.005.
41. Wade, H.E. and Robinson, H.K. (1966) Magnesium ion-independent ribonucleic acid depolymerases in bacteria. Biochem. J. 101, 467-479 doi:10.1042/bj1010467.
42. Estrozi, L.F., Boehringer, D., Shan, S.-o., Ban, N. and Schaffitzel, C. (2011) Cryo-EM structure of the E. coli translating ribosome in complex with SRP and its receptor. Nat. Struct. Mol. Biol. 18, 88-90 doi:10.1038/nsmb.1952.
43. Duong, F. and Wickner, W. (1997) Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. 16, 2756-2768 doi:10.1093/emboj/16.10.2756.
44. Miroux, B. and Walker, J.E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 doi:10.1006/jmbi.1996.0399.
45. Knowles, T.J., Finka, R., Smith, C., Lin, Y.-P., Dafforn, T. and Overduin, M. (2009) Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J. Am. Chem. Soc. 131, 7484-7485 doi:10.1021/ja810046q.
46. Paulin, S., Jamshad, M., Dafforn, T.R., Garcia-Lara, J., Foster, S.J., Galley, N.F. et al. (2014) Surfactant-free purification of membrane protein complexes from bacteria: application to the staphylococcal penicillin-binding protein complex PBP2/PBP2a. Nanotechnology 25, 285101 doi:10.1088/0957-4484/25/28/285101.
47. Rajesh, S., Knowles, T. and Overduin, M. (2011) Production of membrane proteins without cells or detergents. New Biotechnol. 28, 250-254 doi:10.1016/j.nbt.2010.07.011.
48. Osborne, A.R. and Rapoport, T.A. (2007) Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 129, 97-110 doi:10.1016/j.cell.2007.02.036.
49. Kohler, R., Boehringer, D., Greber, B., Bingel-Erlenmeyer, R., Collinson, I., Schaffitzel, C. et al. (2009) YidC and Oxa1 form dimeric insertion pores on the translating ribosome. Mol. Cell 34, 344-353 doi:10.1016/j.molcel.2009.04.019.
50. Deckers-Hebestreit, G. and Altendorf, K. (1992) The Fo complex of the proton-translocating F-type ATPase of Escherichia coli. J. Exp. Biol. 172, 451-459 PMID: 1337099.
51. Foster, D.L. and Fillingame, R.H. (1982) Stoichiometry of subunits in the H+-ATPase complex of Escherichia coli. J. Biol. Chem. 257, 2009-2015 PMID: 6460031.
52. Chang, G., Spencer, R.H., Lee, A.T., Barclay, M.T. and Rees, D.C. (1998) Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science 282, 2220-2226 doi:10.1126/science.282.5397.2220.
53. Corey, R.A., Allen, W.J. and Collinson, I. (2016) Protein translocation: what's the problem? Biochem. Soc. Trans. 44, 753-759 doi:10.1042/BST20160047.
54. Yi, L., Jiang, F., Chen, M., Cain, B., Bolhuis, A. and Dalbey, R.E. (2003) YidC is strictly required for membrane insertion of subunits a and c of the F1F0ATP synthase and SecE of the SecYEG translocase. Biochemistry 42, 10537-10544 doi:10.1021/bi034309h.
55. Yuan, J., Phillips, G.J. and Dalbey, R.E. (2007) 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, 8961-8972 doi:10.1128/JB.01365-07.
56. Koch, H.-G., Moser, M., Schimz, K.-L. and Muller, M. (2002) The integration of YidC into the cytoplasmic membrane of Escherichia coli requires the signal recognition particle, SecA and SecYEG. J. Biol. Chem. 277, 5715-5718 doi:10.1074/jbc.C100683200.
57. Baars, L., Wagner, S., Wickstrom, D., Klepsch, M., Ytterberg, A.J., van Wijk, K.J. et al. (2008) Effects of SecE depletion on the inner and outer membrane proteomes of Escherichia coli. J. Bacteriol. 190, 3505-3525 doi:10.1128/JB.01631-07.
58. Robinson, P.J. and Woolhead, C.A. (2013) Post-translational membrane insertion of an endogenous YidC substrate. Biochim. Biophys. Acta, Mol. Cell Res. 1833, 2781-2788 doi:10.1016/j.bbamcr.2013.07.003.
59. Scotti, P.A., Urbanus, M.L., Brunner, J., de Gier, J.-W.L., von Heijne, G., van der Does, C. et al. (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549 doi:10.1093/emboj/19.4.542.
60. Urbanus, M.L., Fröderberg, L., Drew, D., Björk, P., de Gier, J.-W.L., Brunner, J. et al. (2002) Targeting, insertion, and localization of Escherichia coli YidC. J. Biol. Chem. 277, 12718-12723 doi:10.1074/jbc.M200311200.
61. Driessen, A.J. (1994) How proteins cross the bacterial cytoplasmic membrane. J. Membr. Biol. 142, 145-159 doi:10.1007/BF00234937.
62. Li, G.-W., Burkhardt, D., Gross, C. and Weissman, J.S. (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157, 624-635 doi:10.1016/j.cell.2014.02.033.
63. Pfeffer, S., Burbaum, L., Unverdorben, P., Pech, M., Chen, Y., Zimmermann, R. et al. (2015) Structure of the native Sec61 protein-conducting channel. Nat. Commun. 6, 8403 doi:10.1038/ncomms9403.
64. Tsukazaki, T., Mori, H., Echizen, Y., Ishitani, R., Fukai, S., Tanaka, T. et al. (2011) Structure and function of a membrane component SecDF that enhances protein export. Nature 474, 235-238 doi:10.1038/nature09980.
65. Komar, J., Botte, M., Collinson, I., Schaffitzel, C. and Berger, I. (2015) ACEMBLing a multiprotein transmembrane complex: the functional SecYEG-SecDF-YajC-YidC holotranslocon protein secretase/insertase. Methods Enzymol. 556, 23-49 doi:10.1016/bs.mie.2014.12.027.