YfgM is an ancillary subunit of the secyeg translocon in escherichia coli

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 19089-19097

  Götzke, Hansjörg ^a   Palombo, Isolde ^a   Muheim, Claudio ^a   Perrody, Elsa ^b   Genevaux, Pierre ^b   Kudva, Renuka ^c,d   Müller, Matthias ^c,d   Daley, Daniel O ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UPS   (France)

^c Institute of Biochemistry and Molecular Biology Zentrum für Biochemie und Molekulare   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

PERIPLASMIC CHAPERONE; PROTEIN SECRETION; PROTEIN TRANSFER; TRANSLOCON;

ESCHERICHIA COLI;

CHAPERONE; DEGP PROTEIN; FKPA PROTEIN; MEMBRANE PROTEIN; PPID PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN; SECYEG TRANSLOCON; SURA PROTEIN; TRANSLOCON; UNCLASSIFIED DRUG; YFGM PROTEIN;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; IMMUNOPRECIPITATION; NONHUMAN; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PURIFICATION;

BN-PAGE; ESCHERICHIA COLI (E. COLI); MEMBRANE BIOGENESIS; MEMBRANE PROTEIN; PERIPLASMIC CHAPERONES; PROTEIN SECRETION; PROTEIN TRANSLOCATION; SECYEG TRANSLOCON;

CELL MEMBRANE; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; MOLECULAR CHAPERONES; OXIDATIVE STRESS; PERIPLASM; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

EID: 84903842242     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.541672     Document Type: Article

References (58)

1. Dalbey, R. E., and Kuhn, A. (2012) Protein traffic in Gram-negative bacteria: how exported and secreted proteins find their way. FEMS Microbiol. Rev. 36, 1023-1045
2. Economou, A. (2000) Bacterial protein translocase: a unique molecular machine with an army of substrates. FEBS Lett. 476, 18-21
3. Park, E., and Rapoport, T. A. (2012) Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41, 21-40
4. Rapoport, T. A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669
5. du Plessis, D. J., Nouwen, N., and Driessen, A. J. (2011) The Sec translocase. Biochim. Biophys. Acta 1808, 851-865
6. Lycklama A Nijeholt, J. A., and Driessen, A. J. (2012) The bacterial Sectranslocase: structure and mechanism. Philos. Trans. R Soc. Lond. B Biol. Sci. 367, 1016-1028
7. Dautin, N., and Bernstein, H. D. (2007) Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61, 89-112
8. Leyton, D. L., Rossiter, A. E., and Henderson, I. R. (2012) From self-sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat. Rev. Microbiol. 10, 213-225
9. Okuda, S., and Tokuda, H. (2011) Lipoprotein sorting in bacteria. Annu. Rev. Microbiol. 65, 239-259
10. Rigel, N. W., and Silhavy, T. J. (2012) Making a-barrel: assembly of outer membrane proteins in Gram-negative bacteria. Curr. Opin. Microbiol. 15, 189-193
11. Ruiz, N., Kahne, D., and Silhavy, T. J. (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4, 57-66
12. Egea, P. F., and Stroud, R. M. (2010) Lateral opening of a translocon upon entry of protein suggests the mechanism of insertion into membranes. Proc. Natl. Acad. Sci. U. S. A. 107, 17182-17187
13. Tsukazaki, T., Mori, H., Fukai, S., Ishitani, R., Mori, T., Dohmae, N., Perederina, A., Sugita, Y., Vassylyev, D. G., Ito, K., and Nureki, O. (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455, 988-991
14. 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 proteinconducting channel. Nature 427, 36-44
15. 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
16. Samuelson, J. C., Chen, M., Jiang, F., Möller, I., Wiedmann, M., Kuhn, A., Phillips, G. J., and Dalbey, R. E. (2000) YidC mediates membrane protein insertion in bacteria. Nature 406, 637-641
17. Scotti, P. A., Urbanus, M. L., Brunner, J., de Gier, J. W., von Heijne, G., van der Does, C., Driessen, A. J., Oudega, B., and Luirink, J. (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549
18. Sachelaru, I., Petriman, N. A., Kudva, R., Kuhn, P., Welte, T., Knapp, B., Drepper, F., Warscheid, B., and Koch, H. G. (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
19. Duong, F., and Wickner, W. (1997) The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. 16, 4871-4879
20. Tsukazaki, T., Mori, H., Echizen, Y., Ishitani, R., Fukai, S., Tanaka, T., Perederina, A., Vassylyev, D. G., Kohno, T., Maturana, A. D., Ito, K., and Nureki, O. (2011) Structure and function of a membrane component SecDF that enhances protein export. Nature 474, 235-238
21. 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
22. Boy, D., and Koch, H. G. (2009) Visualization of distinct entities of the SecYEG translocon during translocation and integration of bacterial proteins. Mol. Biol. Cell 20, 1804-1815
23. Maddalo, G., Stenberg-Bruzell, F., Götzke, H., Toddo, S., Björkholm, P., Eriksson, H., Chovanec, P., Genevaux, P., Lehtiö, J., Ilag, L. L., and Daley, D. O. (2011) Systematic analysis of native membrane protein complexes in Escherichia coli. J. Proteome Res. 10, 1848-1859
24. Antonoaea, R., Fürst, M., Nishiyama, K., and Müller, M. (2008) The periplasmic chaperone PpiD interacts with secretory proteins exiting from the SecYEG translocon. Biochemistry 47, 5649-5656
25. Toddo, S., Söderström, B., Palombo, I., von Heijne, G., Nørholm, M. H., and Daley, D. O. (2012) Application of split-green fluorescent protein for topology mapping membrane proteins in Escherichia coli. Protein Sci. 21, 1571-1576
26. Dartigalongue, C., and Raina, S. (1998) A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17, 3968-3980
27. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006. 0008
28. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97, 6640-6645
29. Stenberg, F., Chovanec, P., Maslen, S. L., Robinson, C. V., Ilag, L. L., von Heijne, G., and Daley, D. O. (2005) Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 280, 34409-34419
30. Zaslaver, A., Bren, A., Ronen, M., Itzkovitz, S., Kikoin, I., Shavit, S., Liebermeister, W., Surette, M. G., and Alon, U. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat. Methods 3, 623-628
31. Daley, D. O., Rapp, M., Granseth, E., Melén, K., Drew, D., and von Heijne, G. (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321-1323
32. Rapp, M., Drew, D., Daley, D. O., Nilsson, J., Carvalho, T., Melén, K., De Gier, J. W., and Von Heijne, G. (2004) Experimentally based topology models for E. coli inner membrane proteins. Protein Sci. 13, 937-945
33. Cajo, G. C., Horne, B. E., Kelley, W. L., Schwager, F., Georgopoulos, C., and Genevaux, P. (2006) The role of the DIF motif of the DnaJ (Hsp40) cochaperone in the regulation of the DnaK (Hsp70) chaperone cycle. J. Biol. Chem. 281, 12436-12444
34. Perrody, E., Cirinesi, A. M., Desplats, C., Keppel, F., Schwager, F., Tranier, S., Georgopoulos, C., and Genevaux, P. (2012) bacteriophage-encoded J-domain protein interacts with the DnaK/Hsp70 chaperone and stabilizes the heat-shock factor -32 of Escherichia coli. PLoS Genet. 8, e1003037
35. Bordes, P., Cirinesi, A. M., Ummels, R., Sala, A., Sakr, S., Bitter, W., and Genevaux, P. (2011) SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 108, 8438-8443
36. Ricci, D. P., and Silhavy, T. J. (2012) The Bam machine: a molecular cooper. Biochim. Biophys. Acta 1818, 1067-1084
37. Matern, Y., Barion, B., and Behrens-Kneip, S. (2010) PpiD is a player in the network of periplasmic chaperones in Escherichia coli. BMC Microbiol. 10, 251
38. Liu, A., Tran, L., Becket, E., Lee, K., Chinn, L., Park, E., Tran, K., and Miller, J. H. (2010) Antibiotic sensitivity profiles determined with an Escherichia coli gene knockout collection: generating an antibiotic bar code. Antimicrob. Agents Chemother. 54, 1393-1403
39. Lazar, S. W., and Kolter, R. (1996) SurA assists the folding of Escherichia coli outer membrane proteins. J. Bacteriol. 178, 1770-1773
40. Rouvière, P. E., and Gross, C. A. (1996) SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 10, 3170-3182
41. Schwalm, J., Mahoney, T. F., Soltes, G. R., and Silhavy, T. J. (2013) Role for Skp in LptD Assembly in Escherichia coli. J. Bacteriol. 195, 3734-3742
42. Rizzitello, A. E., Harper, J. R., and Silhavy, T. J. (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J. Bacteriol. 183, 6794-6800
43. Alba, B. M., and Gross, C. A. (2004) Regulation of the Escherichia coli -dependent envelope stress response. Mol. Microbiol. 52, 613-619
44. Raivio, T. L., and Silhavy, T. J. (2001) Periplasmic stress and ECF - factors. Annu. Rev Microbiol. 55, 591-624
45. Ruiz, N., and Silhavy, T. J. (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8, 122-126
46. Rowley, G., Spector, M., Kormanec, J., and Roberts, M. (2006) Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4, 383-394
47. Gardel, C., Benson, S., Hunt, J., Michaelis, S., and Beckwith, J. (1987) secD, a new gene involved in protein export in Escherichia coli. J. Bacteriol. 169, 1286-1290
48. Gardel, C., Johnson, K., Jacq, A., and Beckwith, J. (1990) The secD locus of E. coli codes for two membrane proteins required for protein export. EMBO J. 9, 4205-4206
49. Fang, J., and Wei, Y. (2011) Expression, purification and characterization of the Escherichia coli integral membrane protein YajC. Protein Pept. Lett. 18, 601-608
50. Nouwen, N., and Driessen, A. J. (2002) SecDFyajC forms a heterotetrameric complex with YidC. Mol. Microbiol. 44, 1397-1405
51. Kato, Y., Nishiyama, K., and Tokuda, H. (2003) Depletion of SecDF-YajC causes a decrease in the level of SecG: implication for their functional interaction. FEBS Lett. 550, 114-118
52. Schägger, H. (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555, 154-159
53. Ieva, R., Tian, P., Peterson, J. H., and Bernstein, H. D. (2011) Sequential and spatially restricted interactions of assembly factors with an autotransporter - domain. Proc. Natl. Acad. Sci. U. S. A. 108, E383-E391
54. Schweiger, R., Müller, N. C., Schmitt, M. J., Soll, J., and Schwenkert, S. (2012) AtTPR7 is a chaperone-docking protein of the Sec translocon in Arabidopsis. J. Cell Sci. 125, 5196-5207
55. Cerveny, L., Straskova, A., Dankova, V., Hartlova, A., Ceckova, M., Staud, F., and Stulik, J. (2013) Tetratricopeptide repeat motifs in the world of bacterial pathogens: role in virulence mechanisms. Infect. Immun. 81, 629-635
56. Westphal, K., Langklotz, S., Thomanek, N., and Narberhaus, F. (2012) A trapping approach reveals novel substrates and physiological functions of the essential protease FtsH in Escherichia coli. J. Biol. Chem. 287, 42962-42971
57. Zhang, M., Lin, S., Song, X., Liu, J., Fu, Y., Ge, X., Fu, X., Chang, Z., and Chen, P. R. (2011) A genetically incorporated crosslinker reveals chaperone cooperation in acid resistance. Nat. Chem. Biol. 7, 671-677
58. Akiyama, Y., and Ito, K. (1990) SecY protein, a membrane-embedded secretion factor of E. coli, is cleaved by the ompT protease in vitro. Biochem. Biophys. Res. Commun. 167, 711-715