Multitasking SecB chaperones in bacteria

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Sala, Ambre ^a   Bordes, Patricia ^a   Genevaux, Pierre ^a  

^a UPS   (France)

Author keywords

DnaK; Proteases; Protein folding and targeting; SecA; Toxin antitoxins; Trigger factor

Indexed keywords

ANTITOXIN; CHAPERONIN 60; PROTEIN DNAK; PROTEIN SECB; TOXIN;

BACTERIA; CELL FUNCTION; ELECTRON SPIN RESONANCE; ESCHERICHIA COLI; GENE MUTATION; GROWTH INHIBITION; INTRACELLULAR TRANSPORT; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN TARGETING; PROTEOMICS; REVIEW;

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA; PROTEOBACTERIA;

EID: 84920651078     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00666     Document Type: Review

References (129)

1. Agashe, V. R., Guha, S., Chang, H. C., Genevaux, P., Hayer-Hartl, M., Stemp, M.,et al. (2004). Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell 117, 199-209. doi: 10.1016/S0092-8674(04)00299-5
2. Altman, E., Kumamoto, C. A., and Emr, S. D. (1991). Heat-shock proteins can substitute for SecB function during protein export in Escherichia coli. EMBO J. 10, 239-245.
3. Baars, L., Ytterberg, A. J., Drew, D., Wagner, S., Thilo, C., Van Wijk, K. J.,et al. (2006). Defining the role of the Escherichia coli chaperone SecB using comparative proteomics. J. Biol. Chem. 281, 10024-10034. doi: 10.1074/jbc. M509929200
4. Babu, M., Diaz-Mejia, J. J., Vlasblom, J., Gagarinova, A., Phanse, S., Graham, C.,et al. (2011). Genetic interaction maps in Escherichia coli reveal functional crosstalk among cell envelope biogenesis pathways. PLoS Genet. 7:e1002377. doi: 10.1371/journal.pgen.1002377
5. Bechtluft, P., Nouwen, N., Tans, S. J., and Driessen, A. J. M. (2010). SecB-a chaperone dedicated to protein translocation. Mol. Biosyst. 6, 620-627. doi: 10.1039/b915435c
6. Bechtluft, P., Van Leeuwen, R. G. H., Tyreman, M., Tomkiewicz, D., Nouwen, N., Tepper, H. L.,et al. (2007). Direct observation of chaperone-induced changes in a protein folding pathway. Science 318, 1458-1461. doi: 10.1126/science.1144972
7. Bordes, P., Cirinesi, A. M., Ummels, R., Sala, A., Sakr, S., Bitter, W.,et al. (2011). SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 108, 8438-8443. doi: 10.1073/pnas.1101189108
8. Brehmer, D., Rudiger, S., Gassler, C. S., Klostermeier, D., Packschies, L., Reinstein, J.,et al. (2001). Tuning of chaperone activity of Hsp70 proteins by modulation of nucleotide exchange. Nat. Struct. Biol. 8, 427-432. doi: 10.1038/87588
9. Bukau, B., Deuerling, E., Pfund, C., and Craig, E. A. (2000). Getting newly synthesized proteins into shape. Cell 101, 119-122. doi: 10.1016/S0092-8674(00)80806-5
10. Calloni, G., Chen, T., Schermann, S. M., Chang, H. C., Genevaux, P., Agostini, F.,et al. (2012). DnaK functions as a central hub in the E. coli chaperone network. Cell Rep. 1, 251-264. doi: 10.1016/j.celrep.2011.12.007
11. Castanie-Cornet, M. P., Bruel, N., and Genevaux, P. (2014). Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane. Biochim. Biophys. Acta 1843, 1442-1456. doi: 10.1016/j.bbamcr.2013.11.007
12. Chatzi, K. E., Sardis, M. F., Karamanou, S., and Economou, A. (2013). Breaking on through to the other side: protein export through the bacterial Sec system. Biochem. J. 449, 25-37. doi: 10.1042/BJ20121227
13. Collier, D. N., Bankaitis, V. A., Weiss, J. B., and Bassford, P. J. Jr. (1988). The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell 53, 273-283. doi: 10.1016/0092-8674(88)90389-3
14. Crane, J. M., Mao, C. F., Lilly, A. A., Smith, V. F., Suo, Y. Y., Hubbell, W. L.,et al. (2005). Mapping of the docking of SecA onto the chaperone SecB by site-directed spin labeling: insight into the mechanism of ligand transfer during protein export. J. Mol. Biol. 353, 295-307. doi: 10.1016/j.jmb.2005.08.022
15. Crane, J. M., Suo, Y. Y., Lilly, A. A., Mao, C. F., Hubbell, W. L., and Randall, L. L. (2006). Sites of interaction of a precursor polypeptide on the export chaperone SecB mapped by site-directed spin labeling. J. Mol. Biol. 363, 63-74. doi: 10.1016/j.jmb.2006.07.021
16. Crooke, E., Brundage, L., Rice, M., and Wickner, W. (1988a). ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes. EMBO J. 7, 1831-1835.
17. Crooke, E., Guthrie, B., Lecker, S., Lill, R., and Wickner, W. (1988b). ProOmpA is stabilized for membrane translocation by either purified E. coli trigger factor or canine signal recognition particle. Cell 54, 1003-1011. doi: 10.1016/0092-8674(88)90115-8
18. Crooke, E., and Wickner, W. (1987). Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form. Proc. Natl. Acad. Sci. U.S.A. 84, 5216-5220. doi: 10.1073/pnas.84.15.5216
19. Dalbey, R. E., Wang, P., and Kuhn, A. (2011). Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 80, 161-187. doi: 10.1146/annurev-biochem-060409-092524
20. Danese, P. N., Murphy, C. K., and Silhavy, T. J. (1995). Multicopy suppression of cold-sensitive sec mutations in Escherichia coli. J. Bacteriol. 177, 4969-4973.
21. Debarbieux, L., and Wandersman, C. (2001). Folded HasA inhibits its own secretion through its ABC exporter. EMBO J. 20, 4657-4663. doi: 10.1093/emboj/20.17.4657
22. Dekker, C., De Kruijff, B., and Gros, P. (2003). Crystal structure of SecB from Escherichia coli. J. Struct. Biol. 144, 313-319. doi: 10.1016/j.jsb.2003.09.012
23. Delepelaire, P. (2004). Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 1694, 149-161. doi: 10.1016/j.bbamcr.2004.05.001
24. Delepelaire, P., and Wandersman, C. (1998). The SecB chaperone is involved in the secretion of the Serratia marcescens HasA protein through an ABC transporter. EMBO J. 17, 936-944. doi: 10.1093/emboj/17.4.936
25. den Blaauwen, T., Terpetschnig, E., Lakowicz, J. R., and Driessen, A. J. (1997). Interaction of SecB with soluble SecA. FEBS Lett. 416, 35-38. doi: 10.1016/S0014-5793(97)01142-3
26. Derman, A. I., Puziss, J. W., Bassford, P. J. Jr., and Beckwith, J. (1993). A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J. 12, 879-888.
27. Deuerling, E., Schulze-Specking, A., Tomoyasu, T., Mogk, A., and Bukau, B. (1999). Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400, 693-696. doi: 10.1038/23301
28. du Plessis, D. J., Nouwen, N., and Driessen, A. J. (2011). The Sec translocase. Biochim. Biophys. Acta 1808, 851-865. doi: 10.1016/j.bbamem.2010.08.016
29. Fekkes, P., De Wit, J. G., Boorsma, A., Friesen, R. H., and Driessen, A. J. (1999). Zinc stabilizes the SecB binding site of SecA. Biochemistry 38, 5111-5116. doi: 10.1021/bi982818r
30. Fekkes, P., De Wit, J. G., Van Der Wolk, J. P., Kimsey, H. H., Kumamoto, C. A., and Driessen, A. J. (1998). Preprotein transfer to the Escherichia coli translocase requires the co-operative binding of SecB and the signal sequence to SecA. Mol. Microbiol. 29, 1179-1190. doi: 10.1046/j.1365-2958.1998.00997.x
31. Fekkes, P., Van Der Does, C., and Driessen, A. J. (1997). The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J. 16, 6105-6113. doi: 10.1093/emboj/16.20.6105
32. Ferbitz, L., Maier, T., Patzelt, H., Bukau, B., Deuerling, E., and Ban, N. (2004). Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431, 590-596. doi: 10.1038/nature02899
33. Francetic, O., Hanson, M. P., and Kumamoto, C. A. (1993). PrlA suppression of defective export of maltose-binding protein in SecB mutants of Escherichia coli. J. Bacteriol. 175, 4036-4044.
34. Gannon, P. M., and Kumamoto, C. A. (1993). Mutations of the molecular chaperone protein SecB which alter the interaction between Secb and maltose-binding protein. J. Biol. Chem. 268, 1590-1595.
35. Gannon, P. M., Li, P., and Kumamoto, C. A. (1989). The mature portion of Escherichia coli maltose-binding protein (MBP) determines the dependence of MBP on SecB for export. J. Bacteriol. 171, 813-818.
36. Genevaux, P., Georgopoulos, C., and Kelley, W. L. (2007). The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol. Microbiol. 66, 840-857. doi: 10.1111/j.1365-2958.2007.05961.x
37. Genevaux, P., Keppel, F., Schwager, F., Langendijk-Genevaux, P. S., Hartl, F. U., and Georgopoulos, C. (2004). In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep. 5, 195-200. doi: 10.1038/sj.embor.7400067
38. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. (2005). Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371-382. doi: 10.1038/nrmicro1147
39. Goeders, N., and Van Melderen, L. (2014). Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6, 304-324. doi: 10.3390/toxins6010304
40. Gouridis, G., Karamanou, S., Gelis, I., Kalodimos, C. G., and Economou, A. (2009). Signal peptides are allosteric activators of the protein translocase. Nature 462, 363-367. doi: 10.1038/nature08559
41. Grabowicz, M., Yeh, J., and Silhavy, T. J. (2013). Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel. J. Bacteriol. 195, 1327-1334. doi: 10.1128/JB.02142-12
42. Gupta, A. (2009). Killing activity and rescue function of genome-wide toxin-antitoxin loci of Mycobacterium tuberculosis. FEMS Microbiol. Lett. 290, 45-53. doi: 10.1111/j.1574-6968.2008.01400.x
43. Guthrie, B., and Wickner, W. (1990). Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol. 172, 5555-5562.
44. Hardy, S. J., and Randall, L. L. (1991). A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443. doi: 10.1126/science.1989077
45. Harrison, C. J., Hayer-Hartl, M., Di Liberto, M., Hartl, F., and Kuriyan, J. (1997). Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276, 431-435. doi: 10.1126/science.276.5311.431
46. Hartl, F. U., Lecker, S., Schiebel, E., Hendrick, J. P., and Wickner, W. (1990). The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 63, 269-279. doi: 10.1016/0092-8674(90)90160-G
47. Hayashi, S., and Wu, H. C. (1985). Accumulation of prolipoprotein in Escherichia coli mutants defective in protein secretion. J. Bacteriol. 161, 949-954.
48. Hoffmann, A., Becker, A. H., Zachmann-Brand, B., Deuerling, E., Bukau, B., and Kramer, G. (2012). Concerted action of the ribosome and the associated chaperone trigger factor confines nascent polypeptide folding. Mol. Cell 48, 63-74. doi: 10.1016/j.molcel.2012.07.018
49. Hoffmann, A., Bukau, B., and Kramer, G. (2010). Structure and function of the molecular chaperone Trigger Factor. Biochim. Biophys. Acta 1803, 650-661. doi: 10.1016/j.bbamcr.2010.01.017
50. Holland, I. B., Schmitt, L., and Young, J. (2005). Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol. Membr. Biol. 22, 29-39. doi: 10.1080/09687860500042013
51. Huber, D., Rajagopalan, N., Preissler, S., Rocco, M. A., Merz, F., Kramer, G.,et al. (2011). SecA interacts with ribosomes in order to facilitate posttranslational translocation in bacteria. Mol. Cell 41, 343-353. doi: 10.1016/j.molcel.2010.12.028
52. Jin, T., and Inouye, M. (1995). Identification of the genes in multicopy plasmids affecting ompC and ompF expression in Escherichia coli. FEMS Microbiol. Lett. 133, 225-231. doi: 10.1111/j.1574-6968.1995.tb07889.x
53. Kaiser, C. M., Chang, H. C., Agashe, V. R., Lakshmipathy, S. K., Etchells, S. A., Hayer-Hartl, M.,et al. (2006). Real-time observation of trigger factor function on translating ribosomes. Nature 444, 455-460. doi: 10.1038/nature05225
54. Karamyshev, A. L., and Johnson, A. E. (2005). Selective SecA association with signal sequences in ribosome-bound nascent chains: a potential role for SecA in ribosome targeting to the bacterial membrane. J. Biol. Chem. 280, 37930-37940. doi: 10.1074/jbc. M509100200
55. Kerner, M. J., Naylor, D. J., Ishihama, Y., Maier, T., Chang, H. C., Stines, A. P.,et al. (2005). Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220. doi: 10.1016/j.cell.2005.05.028
56. Khisty, V. J., Munske, G. R., and Randall, L. L. (1995). Mapping of the binding frame for the chaperone SecB within a natural ligand, galactose-binding protein. J. Biol. Chem. 270, 25920-25927. doi: 10.1074/jbc.270.43.25920
57. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., and Hartl, F. U. (2013). Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355. doi: 10.1146/annurev-biochem-060208-092442
58. Kimsey, H. H., Dagarag, M. D., and Kumamoto, C. A. (1995). Diverse effects of mutation on the activity of the Escherichia coli export chaperone SecB. J. Biol. Chem. 270, 22831-22835. doi: 10.1074/jbc.270.39.22831
59. Knoblauch, N. T., Rudiger, S., Schonfeld, H. J., Driessen, A. J., Schneider-Mergener, J., and Bukau, B. (1999). Substrate specificity of the SecB chaperone. J. Biol. Chem. 274, 34219-34225. doi: 10.1074/jbc.274.48.34219
60. Kramer, G., Boehringer, D., Ban, N., and Bukau, B. (2009). The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597. doi: 10.1038/nsmb.1614
61. Kramer, G., Rauch, T., Rist, W., Vorderwulbecke, S., Patzelt, H., Schulze-Specking, A.,et al. (2002). L23 protein functions as a chaperone docking site on the ribosome. Nature 419, 171-174. doi: 10.1038/nature01047
62. Kumamoto, C. A., and Beckwith, J. (1983). Mutations in a new gene, secB, cause defective protein localization in Escherichia coli. J. Bacteriol. 154, 253-260.
63. Kumamoto, C. A., and Beckwith, J. (1985). Evidence for specificity at an early step in protein export in Escherichia coli. J. Bacteriol. 163, 267-274.
64. Kusters, I., Van Den Bogaart, G., Kedrov, A., Krasnikov, V., Fulyani, F., Poolman, B.,et al. (2011). Quaternary structure of SecA in solution and bound to SecYEG probed at the single molecule level. Structure 19, 430-439. doi: 10.1016/j.str.2010.12.016
65. Kusters, R., De Vrije, T., Breukink, E., and De Kruijff, B. (1989). SecB protein stabilizes a translocation-competent state of purified prePhoE protein. J. Biol. Chem. 264, 20827-20830.
66. Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y., and Ito, K. (1989). Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J. 8, 3517-3521.
67. Laminet, A. A., Kumamoto, C. A., and Pluckthun, A. (1991). Folding in vitro and transport in vivo of pre-Beta-Lactamase are SecB independent. Mol. Microbiol. 5, 117-122. doi: 10.1111/j.1365-2958.1991.tb01832.x
68. Lecker, S., Lill, R., Ziegelhoffer, T., Georgopoulos, C., Bassford, P. J., Kumamoto, C. A.,et al. (1989). Three pure chaperone proteins of Escherichia coli SecB, trigger factor and groel-form soluble complexes with precursor proteins in vitro. EMBO J. 8, 2703-2709.
69. Lee, H. C., and Bernstein, H. D. (2002). Trigger factor retards protein export in Escherichia coli. J. Biol. Chem. 277, 43527-43535. doi: 10.1074/jbc. M205950200
70. Letoffe, S., Ghigo, J. M., and Wandersman, C. (1994). Secretion of the Serratia marcescens HasA protein by an ABC transporter. J. Bacteriol. 176, 5372-5377.
71. Lewis, K. (2010). Persister cells. Annu. Rev. Microbiol. 64, 357-372. doi: 10.1146/annurev.micro.112408.134306
72. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991). Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. U.S.A. 88, 2874-2878. doi: 10.1073/pnas.88.7.2874
73. Lill, R., Crooke, E., Guthrie, B., and Wickner, W. (1988). The "trigger factor cycle" includes ribosomes, presecretory proteins, and the plasma membrane. Cell 54, 1013-1018. doi: 10.1016/0092-8674(88)90116-X
74. Liu, G., Topping, T. B., and Randall, L. L. (1989). Physiological role during export for the retardation of folding by the leader peptide of maltose-binding protein. Proc. Natl. Acad. Sci. U.S.A. 86, 9213-9217. doi: 10.1073/pnas.86.23.9213
75. Luirink, J., and Sinning, I. (2004). SRP-mediated protein targeting: structure and function revisited. Biochim. Biophys. Acta 1694, 17-35. doi: 10.1016/j.bbamcr.2004.03.013
76. Mah, N., Perez-Iratxeta, C., and Andrade-Navarro, M. A. (2010). Outer membrane pore protein prediction in mycobacteria using genomic comparison. Microbiology 156, 2506-2515. doi: 10.1099/mic.0.040089-0
77. Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2009). Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4, 19. doi: 10.1186/1745-6150-4-19
78. Marani, P., Wagner, S., Baars, L., Genevaux, P., De Gier, J. W., Nilsson, I.,et al. (2006). New Escherichia coli outer membrane proteins identified through prediction and experimental verification. Protein Sci. 15, 884-889. doi: 10.1110/ps.051889506
79. Margolis, J. J., El-Etr, S., Joubert, L. M., Moore, E., Robison, R., Rasley, A.,et al. (2010). Contributions of Francisella tularensis subsp. novicida chitinases and Sec secretion system to biofilm formation on chitin. Appl. Environ. Microbiol. 76, 596-608. doi: 10.1128/AEM.02037-09
80. Mcfarland, L., Francetic, O., and Kumamoto, C. A. (1993). A mutation of Escherichia coli SecA protein that partially compensates for the absence of SecB. J. Bacteriol. 175, 2255-2262.
81. Miller, A., Wang, L., and Kendall, D. A. (2002). SecB modulates the nucleotide-bound state of SecA and stimulates ATPase activity. Biochemistry 41, 5325-5332. doi: 10.1021/bi025639p
82. Muller, J. P. (1996). Influence of impaired chaperone or secretion function on SecB production in Escherichia coli. J. Bacteriol. 178, 6097-6104.
83. Muren, E. M., Suciu, D., Topping, T. B., Kumamoto, C. A., and Randall, L. L. (1999). Mutational alterations in the homotetrameric chaperone SecB that implicate the structure as dimer of dimers. J. Biol. Chem. 274, 19397-19402. doi: 10.1074/jbc.274.27.19397
84. Nichols, R. J., Sen, S., Choo, Y. J., Beltrao, P., Zietek, M., Chaba, R.,et al. (2011). Phenotypic landscape of a bacterial cell. Cell 144, 143-156. doi: 10.1016/j.cell.2010.11.052
85. O'Brien, E. P., Christodoulou, J., Vendruscolo, M., and Dobson, C. M. (2012). Trigger factor slows co-translational folding through kinetic trapping while sterically protecting the nascent chain from aberrant cytosolic interactions. J. Am. Chem. Soc. 134, 10920-10932. doi: 10.1021/ja302305u
86. Oh, E., Becker, A. H., Sandikci, A., Huber, D., Chaba, R., Gloge, F.,et al. (2011). Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147, 1295-1308. doi: 10.1016/j.cell.2011.10.044
87. Palmer, T., and Berks, B. C. (2012). The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10, 483-496. doi: 10.1038/nrmicro2814
88. Patel, R., Smith, S. M., and Robinson, C. (2014). Protein transport by the bacterial Tat pathway. Biochim. Biophys. Acta 1843, 1620-1628. doi: 10.1016/j.bbamcr.2014.02.013
89. Phillips, G. J., and Silhavy, T. J. (1990). Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature 344, 882-884. doi: 10.1038/344882a0
90. Powers, E. L., and Randall, L. L. (1995). Export of periplasmic galactose-binding protein in Escherichia coli depends on the chaperone SecB. J. Bacteriol. 177, 1906-1907.
91. Qi, H. Y., Hyndman, J. B., and Bernstein, H. D. (2002). DnaK promotes the selective export of outer membrane protein precursors in SecA-deficient Escherichia coli. J. Biol. Chem. 277, 51077-51083. doi: 10.1074/jbc. M209238200
92. Raine, A., Lovmar, M., Wikberg, J., and Ehrenberg, M. (2006). Trigger factor binding to ribosomes with nascent peptide chains of varying lengths and sequences. J. Biol. Chem. 281, 28033-28038. doi: 10.1074/jbc. M605753200
93. Ramage, H. R., Connolly, L. E., and Cox, J. S. (2009). Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet. 5:e1000767. doi: 10.1371/journal.pgen.1000767
94. Randall, L. L., Crane, J. M., Lilly, A. A., Liu, G. P., Mao, C. F., Patel, C. N.,et al. (2005). Asymmetric binding between SecA and SecB two symmetric proteins: implications for function in export. J. Mol. Biol. 348, 479-489. doi: 10.1016/j.jmb.2005.02.036
95. 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. doi: 10.1110/ps.03410104
96. Randall, L. L., and Hardy, S. J. (1995). High selectivity with low specificity: how SecB has solved the paradox of chaperone binding. Trends Biochem. Sci. 20, 65-69. doi: 10.1016/S0968-0004(00)88959-8
97. Randall, L. L., and Hardy, S. J. (2002). SecB, one small chaperone in the complex milieu of the cell. Cell. Mol. Life Sci. 59, 1617-1623. doi: 10.1007/PL00012488
98. Rigel, N. W., Gibbons, H. S., Mccann, J. R., Mcdonough, J. A., Kurtz, S., and Braunstein, M. (2009). The accessory SecA2 system of mycobacteria requires ATP binding and the canonical SecA1. J. Biol. Chem. 284, 9927-9936. doi: 10.1074/jbc. M900325200
99. Rudiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997). Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507. doi: 10.1093/emboj/16.7.1501
100. Saibil, H. R., Fenton, W. A., Clare, D. K., and Horwich, A. L. (2013). Structure and allostery of the chaperonin GroEL. J. Mol. Biol. 425, 1476-1487. doi: 10.1016/j.jmb.2012.11.028
101. Saio, T., Guan, X., Rossi, P., Economou, A., and Kalodimos, C. G. (2014). Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science 344:1250494. doi: 10.1126/science.1250494
102. Sakr, S., Cirinesi, A. M., Ullers, R. S., Schwager, F., Georgopoulos, C., and Genevaux, P. (2010). Lon protease quality control of presecretory proteins in Escherichia coli and its dependence on the SecB and DnaJ (Hsp40) chaperones. J. Biol. Chem. 285, 23504-23512. doi: 10.1074/jbc. M110.133058
103. Sala, A., Bordes, P., Fichant, G., and Genevaux, P. (2013a). "Toxin-antitoxin loci in Mycobacterium tuberculosis," in Prokaryotic Toxin-Antitoxins, ed. K. Gerdes (Berlin: Springer), 295-314.
104. Sala, A., Calderon, V., Bordes, P., and Genevaux, P. (2013b). TAC from Mycobacterium tuberculosis: a paradigm for stress-responsive toxin-antitoxin systems controlled by SecB-like chaperones. Cell Stress Chaperones 18, 129-135. doi: 10.1007/s12192-012-0396-5
105. Sapriel, G., Wandersman, C., and Delepelaire, P. (2002). The N terminus of the HasA protein and the SecB chaperone cooperate in the efficient targeting and secretion of HasA via the ATP-binding cassette transporter. J. Biol. Chem. 277, 6726-6732. doi: 10.1074/jbc. M108632200
106. Sapriel, G., Wandersman, C., and Delepelaire, P. (2003). The SecB chaperone is bifunctional in Serratia marcescens: SecB is involved in the Sec pathway and required for HasA secretion by the ABC transporter. J. Bacteriol. 185, 80-88. doi: 10.1128/JB.185.1.80-88.2003
107. Saraogi, I., and Shan, S. O. (2014). Co-translational protein targeting to the bacterial membrane. Biochim. Biophys. Acta 1843, 1433-1441. doi: 10.1016/j.bbamcr.2013.10.013
108. Schuessler, D. L., Cortes, T., Fivian-Hughes, A. S., Lougheed, K. E., Harvey, E., Buxton, R. S.,et al. (2013). Induced ectopic expression of HigB toxin in Mycobacterium tuberculosis results in growth inhibition, reduced abundance of a subset of mRNAs and cleavage of tmRNA. Mol. Microbiol. 90, 195-207. doi: 10.1111/mmi.12358
109. Shimizu, H., Nishiyama, K., and Tokuda, H. (1997). Expression of gpsA encoding biosynthetic sn-glycerol 3-phosphate dehydrogenase suppresses both the LB- phenotype of a secB null mutant and the cold-sensitive phenotype of a secG null mutant. Mol. Microbiol. 26, 1013-1021. doi: 10.1046/j.1365-2958.1997.6392003.x
110. Singh, R., Kraft, C., Jaiswal, R., Sejwal, K., Kasaragod, V. B., Kuper, J.,et al. (2014). Cryo-electron microscopic structure of SecA protein bound to the 70S ribosome. J. Biol. Chem. 289, 7190-7199.
111. Snyder, W. B., and Silhavy, T. J. (1992). Enhanced export of beta-galactosidase fusion proteins in prlF mutants is Lon dependent. J. Bacteriol. 174, 5661-5668.
112. Sullivan, J. T., Young, E. F., Mccann, J. R., and Braunstein, M. (2012). The Mycobacterium tuberculosis SecA2 system subverts phagosome maturation to promote growth in macrophages. Infect. Immun. 80, 996-1006. doi: 10.1128/IAI.05987-11
113. Teter, S. A., Houry, W. A., Ang, D., Tradler, T., Rockabrand, D., Fischer, G.,et al. (1999). Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97, 755-765. doi: 10.1016/S0092-8674(00)80787-4
114. Trun, N. J., and Silhavy, T. J. (1989). PrlC, a suppressor of signal sequence mutations in Escherichia coli, can direct the insertion of the signal sequence into the membrane. J. Mol. Biol. 205, 665-676. doi: 10.1016/0022-2836(89)90312-4
115. Trun, N. J., Stader, J., Lupas, A., Kumamoto, C., and Silhavy, T. J. (1988). Two cellular components, PrlA and SecB, that recognize different sequence determinants are required for efficient protein export. J. Bacteriol. 170, 5928-5930.
116. Ullers, R. S., Ang, D., Schwager, F., Georgopoulos, C., and Genevaux, P. (2007). Trigger factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 104, 3101-3106. doi: 10.1073/pnas.0608232104
117. Ullers, R. S., Luirink, J., Harms, N., Schwager, F., Georgopoulos, C., and Genevaux, P. (2004). SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 101, 7583-7588. doi: 10.1073/pnas.0402398101
118. Valent, Q. A., Kendall, D. A., High, S., Kusters, R., Oudega, B., and Luirink, J. (1995). Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14, 5494-5505.
119. van der Sluis, E. O., and Driessen, A. J. (2006). Stepwise evolution of the Sec machinery in Proteobacteria. Trends Microbiol. 14, 105-108. doi: 10.1016/j.tim.2006.01.009
120. Watanabe, T., Hayashi, S., and Wu, H. C. (1988). Synthesis and export of the outer membrane lipoprotein in Escherichia coli mutants defective in generalized protein export. J. Bacteriol. 170, 4001-4007.
121. Wei, S. Q., and Stader, J. (1994). A new suppressor of a lamB signal sequence mutation, prlZ1, maps to 69 minutes on the Escherichia coli chromosome. J. Bacteriol. 176, 5704-5710.
122. Wild, J., Altman, E., Yura, T., and Gross, C. A. (1992). DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 6, 1165-1172. doi: 10.1101/gad.6.7.1165
123. Wild, J., Walter, W. A., Gross, C. A., and Altman, E. (1993). Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J. Bacteriol. 175, 3992-3997.
124. Wolff, N., Sapriel, G., Bodenreider, C., Chaffotte, A., and Delepelaire, P. (2003). Antifolding activity of the SecB chaperone is essential for secretion of HasA, a quickly folding ABC pathway substrate. J. Biol. Chem. 278, 38247-38253. doi: 10.1074/jbc. M302322200
125. Woodbury, R. L., Topping, T. B., Diamond, D. L., Suciu, D., Kumamoto, C. A., Hardy, S. J.,et al. (2000). Complexes between protein export chaperone SecB and SecA - Evidence for separate sites on SecA providing binding energy and regulatory interactions. J. Biol. Chem. 275, 24191-24198. doi: 10.1074/jbc. M002885200
126. Xu, Z., Knafels, J. D., and Yoshino, K. (2000). Crystal structure of the bacterial protein export chaperone SecB. Nat. Struct. Biol. 7, 1172-1177. doi: 10.1038/82040
127. Yamaguchi, Y., and Inouye, M. (2011). Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat. Rev. Microbiol. 9, 779-790. doi: 10.1038/nrmicro2651
128. Zhou, J., and Xu, Z. (2003). Structural determinants of SecB recognition by SecA in bacterial protein translocation. Nat. Struct. Biol. 10, 942-947. doi: 10.1038/nsb980
129. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffe, M. (2008). Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680. doi: 10.1128/JB.01919-07