Heat Shock Transcription Factor σ32 Co-opts the Signal Recognition Particle to Regulate Protein Homeostasis in E. coli

PLoS Biology

Volumn 11, Issue 12, 2013, Pages

  Lim, Bentley ^a   Miyazaki, Ryoji ^b   Neher, Saskia ^c,g   Siegele, Deborah A ^d   Ito, Koreaki ^e   Walter, Peter ^c   Akiyama, Yoshinori ^b   Yura, Takashi ^e   Gross, Carol A ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

^e KYOTO SANGYO UNIVERSITY   (Japan)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOCKING PROTEIN; HEAT SHOCK PROTEIN; MEMBRANE PROTEIN; SIGNAL RECOGNITION PARTICLE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DELTA 32; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CELL MEMBRANE; CYTOPLASM; DISPERSION; ESCHERICHIA COLI; FEEDBACK SYSTEM; GENETIC ANALYSIS; HEAT SHOCK RESPONSE; INTRACELLULAR SIGNALING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM;

BACTERIAL OUTER MEMBRANE PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; HOMEOSTASIS; PROTEIN FOLDING; SIGMA FACTOR; SIGNAL RECOGNITION PARTICLE;

EID: 84892779367     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001735     Document Type: Article

References (87)

1. Anckar J, Sistonen L, (2011) Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu Rev Biochem 80: 1089-1115 doi:10.1146/annurev-biochem-060809-095203.
2. Morimoto RI, (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes & Development 22: 1427-1438 doi:10.1101/gad.1657108.
3. Morimoto RI, (2012) The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harbor Symposia on Quantitative Biology 76: 91-99 doi:10.1101/sqb.2012.76.010637.
4. Yamamori T, Yura T, (1980) Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J Bacteriol 142: 843-851.
5. Grossman AD, Erickson JW, Gross CA, (1984) The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38: 383-390.
6. Taylor WE, Straus DB, Grossman AD, Burton ZF, Gross CA, et al. (1984) Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38: 371-381.
7. Straus DB, Walter WA, Gross CA, (1989) The activity of sigma32 is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes & Development 3: 2003-2010 doi:10.1101/gad.3.12a.2003.
8. Straus DB, Walter WA, Gross CA, (1987) The heat shock response of E. coli is regulated by changes in the concentration of σ32. Nature 329: 348-351.
9. Taura T, Kusukawa N, Yura T, Ito K, (1989) Transient shut off of Escherichia coli heat shock protein synthesis upon temperature shift down. Biochem Biophys Res Commun 163: 438-443.
10. Morita M, Kanemori M, Yanagi H, Yura T, (1999) Heat-induced synthesis of sigma32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J Bacteriol 181: 401-410.
11. Morita MT, Tanaka Y, Kodama TS, Kyogoku Y, Yanagi H, et al. (1999) Translational induction of heat shock transcription factor σ32: evidence for a built-in RNA thermosensor. Genes & Development 13: 655.
12. Guisbert E, Yura T, Rhodius VA, Gross CA, (2008) Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiology and Molecular Biology Reviews 72: 545-554 doi:10.1128/MMBR.00007-08.
13. Guisbert E, Herman C, Lu CZ, Gross CA, (2004) A chaperone network controls the heat shock response in E. coli. Genes & Development 18: 2812-2821 doi:10.1101/gad.1219204.
14. Tomoyasu T, Ogura T, Tatsuta T, Bukau B, (1998) Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Mol Microbiol 30: 567-581.
15. Gamer J, Multhaup G, Tomoyasu T, McCarty JS, Rüdiger S, et al. (1996) A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor sigma32. EMBO J 15: 607-617.
16. Gamer J, Bujard H, Bukau B, (1992) Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma32. Cell 69: 833-842.
17. Liberek K, Galitski TP, Zylicz M, Georgopoulos C, (1992) The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the sigma32 transcription factor. Proc Natl Acad Sci USA 89: 3516-3520.
18. Herman C, Thévenet D, D'Ari R, Bouloc P, (1995) Degradation of sigma32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc Natl Acad Sci USA 92: 3516-3520.
19. Kanemori M, Nishihara K, Yanagi H, Yura T, (1997) Synergistic roles of HslVU and other ATP-dependent proteases in controlling in vivo turnover of sigma32 and abnormal proteins in Escherichia coli. J Bacteriol 179: 7219-7225.
20. Tomoyasu T, Gamer J, Bukau B, Kanemori M, Mori H, et al. (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma32. EMBO J 14: 2551-2560.
21. Straus D, Walter W, Gross CA, (1990) DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma32. Genes & Development 4: 2202-2209 doi:10.1101/gad.4.12a.2202.
22. Blaszczak A, Georgopoulos C, Liberek K, (1999) On the mechanism of FtsH-dependent degradation of the sigma32 transcriptional regulator of Escherichia coli and the role of the Dnak chaperone machine. Mol Microbiol 31: 157-166.
23. Horikoshi M, Yura T, Tsuchimoto S, Fukumori Y, Kanemori M, (2004) Conserved region 2.1 of Escherichia coli heat shock transcription factor σ32 is required for modulating both metabolic stability and transcriptional activity. J Bacteriol 186: 7474-7480 doi:10.1128/JB.186.22.7474-7480.2004.
24. Obrist M, Narberhaus F, (2005) Identification of a turnover element in region 2.1 of Escherichia coli sigma32 by a bacterial one-hybrid approach. J Bacteriol 187: 3807-3813 doi:10.1128/JB.187.11.3807-3813.2005.
25. Yura T, Guisbert E, Poritz M, Lu CZ, Campbell E, et al. (2007) Analysis of sigma32 mutants defective in chaperone-mediated feedback control reveals unexpected complexity of the heat shock response. Proc Natl Acad Sci USA 104: 17638-17643 doi:10.1073/pnas.0708819104.
26. Suzuki HH, Ikeda AA, Tsuchimoto SS, Adachi K-IK, Noguchi AA, et al. (2012) Synergistic binding of DnaJ and DnaK chaperones to heat shock transcription factor σ32 ensures its characteristic high metabolic instability: implications for heat shock protein 70 (Hsp70)-Hsp40 mode of function. J Biol Chem 287: 19275-19283 doi:10.1074/jbc.M111.331470.
27. Bernstein HD, Hyndman JB, (2001) Physiological basis for conservation of the signal recognition particle targeting pathway in Escherichia coli. J Bacteriol 183: 2187-2197 doi:10.1128/JB.183.7.2187-2197.2001.
28. Bourgaize DB, Phillips TA, VanBogelen RA, Jones PG, Neidhardt FC, et al. (1990) Loss of 4.5S RNA induces the heat shock response and lambda prophage in Escherichia coli. J Bacteriol 172: 1151-1154.
29. Poritz MA, Bernstein HD, Strub K, Zopf D, Wilhelm H, et al. (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250: 1111-1117.
30. Nonaka G, Blankschien M, Herman C, Gross CA, Rhodius VA, (2006) Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. Genes & Development 20: 1776-1789 doi:10.1101/gad.1428206.
31. Wild J, Kamath-Loeb A, Ziegelhoffer E, Lonetto M, Kawasaki Y, et al. (1992) Partial loss of function mutations in DnaK, the Escherichia coli homologue of the 70-kDa heat shock proteins, affect highly conserved amino acids implicated in ATP binding and hydrolysis. Proc Natl Acad Sci USA 89: 7139-7143.
32. Tomoyasu T, Arsène F, Ogura T, Bukau B, (2001) The C terminus of σ32 is not essential for degradation by FtsH. J Bacteriol 183: 5911-5917 doi:10.1128/JB.183.20.5911-5917.2001.
33. Qi HYH, Bernstein HDH, (1999) SecA is required for the insertion of inner membrane proteins targeted by the Escherichia coli signal recognition particle. J Biol Chem 274: 8993-8997.
34. Schiebel E, Driessen AJ, Hartl FU, Wickner W, (1991) Delta mu H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64: 927-939.
35. van der Wolk JP, de Wit JG, Driessen AJ, (1997) The catalytic cycle of the Escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J 16: 7297-7304 doi:10.1093/emboj/16.24.7297.
36. Hartl FU, Lecker S, Schiebel E, Hendrick JP, 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.
37. Economou A, Wickner W, (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78: 835-843.
38. Neumann-Haefelin C, Schäfer U, Müller M, Koch HG, (2000) SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J 19: 6419-6426 doi:10.1093/emboj/19.23.6419.
39. Wild J, Walter WA, Gross CA, Altman E, (1993) Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J Bacteriol 175: 3992-3997.
40. Oliver DB, Beckwith J, (1981) E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25: 765-772.
41. Schmidt MG, Rollo EE, Grodberg J, Oliver DB, (1988) Nucleotide sequence of the secA gene and secA(Ts) mutations preventing protein export in Escherichia coli. J Bacteriol 170: 3404-3414.
42. Angelini S, Deitermann S, Koch H-G, (2005) FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep 6: 476-481 doi:10.1038/sj.embor.7400385.
43. Kuhn P, Weiche B, Sturm L, Sommer E, Drepper F, et al. (2011) The bacterial SRP receptor, SecA and the ribosome use overlapping binding sites on the SecY translocon. Traffic 12: 563-578 doi:10.1111/j.1600-0854.2011.01167.x.
44. Jiang Y, Cheng Z, Mandon EC, Gilmore R, (2008) An interaction between the SRP receptor and the translocon is critical during cotranslational protein translocation. J Cell Biol 180 (6):: 1149-1161.
45. Mori H, Ito K, (2006) Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc Natl Acad Sci USA 103: 16159-16164 doi:10.1073/pnas.0606390103.
46. Zimmer J, Nam Y, Rapoport TA, (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455: 936-943 doi:10.1038/nature07335.
47. van der Sluis EO, Nouwen N, Koch J, de Keyzer J, van der Does C, et al. (2006) Identification of two interaction sites in SecY that are important for the functional interaction with SecA. J Mol Biol 361: 839-849 doi:10.1016/j.jmb.2006.07.017.
48. Cheng Z, (2004) Identification of cytoplasmic residues of Sec61p involved in ribosome binding and cotranslational translocation. J Cell Biol 168: 67-77 doi:10.1083/jcb.200408188.
49. Becker T, Bhushan S, Jarasch A, Armache JP, Funes S, et al. (2009) Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326: 1369-1373 doi:10.1126/science.1178535.
50. Prinz A, Behrens C, Rapoport TA, Hartmann E, Kalies KU, (2000) Evolutionarily conserved binding of ribosomes to the translocation channel via the large ribosomal RNA. EMBO J 19: 1900-1906 doi:10.1093/emboj/19.8.1900.
51. Shimohata N, Nagamori S, Akiyama Y, Kaback HR, Ito K, (2007) SecY alterations that impair membrane protein folding and generate a membrane stress. J Cell Biol 176: 307-317 doi:10.1083/jcb.200611121.
52. Ito K, Akiyama Y, Yura T, Shiba K, (1986) Diverse effects of the MalE-LacZ hybrid protein on Escherichia coli cell physiology. J Bacteriol 167: 201-204.
53. Manoil C, Beckwith J, (1986) A genetic approach to analyzing membrane protein topology. Science 233: 1403-1408.
54. Prinz WA, Spiess C, Ehrmann M, Schierle C, Beckwith J, (1996) Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase. EMBO J 15: 5209-5217.
55. Serek J, Bauer-Manz G, Struhalla G, van den Berg L, Kiefer D, et al. (2004) Escherichia coli YidC is a membrane insertase for Sec-independent proteins. EMBO J 23: 294-301 doi:10.1038/sj.emboj.7600063.
56. Tatsuta T, Tomoyasu T, Bukau B, Kitagawa M, Mori H, et al. (1998) Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of sigma32 in vivo. Mol Microbiol 30: 583-593.
57. Zhang X, Rashid R, Wang K, Shan S-O, (2010) Sequential checkpoints govern substrate selection during cotranslational protein targeting. Science 328: 757-760 doi:10.1126/science.1186743.
58. Jensen CG, Pedersen S, (1994) Concentrations of 4.5S RNA and Ffh protein in Escherichia coli: the stability of Ffh protein is dependent on the concentration of 4.5S RNA. J Bacteriol 176: 7148-7154.
59. Bukau B, Walker GC, (1990) Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J 9: 4027-4036.
60. Bahl H, Echols H, Straus DB, Court D, Crowl R, et al. (1987) Induction of the heat shock response of E. coli through stabilization of sigma32 by the phage lambda cIII protein. Genes & Development 1: 57-64 doi:10.1101/gad.1.1.57.
61. Petersen TN, Brunak S, Heijne von G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Publishing Group 8: 785-786 doi:10.1038/nmeth.1701.
62. Krogh A, Larsson B, Heijne von G, Sonnhammer ELL, (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol 305: 567-580 doi:10.1006/jmbi.2000.4315.
63. Zylicz M, Nieradko J, Taylor K, (1983) Escherichia coli dnaJ- and dnaK- gene products: synthesis in minicells and membrane-affinity. Biochem Biophys Res Commun 110: 176-180.
64. Bardwell JCJ, Tilly KK, Craig EE, King JJ, Zylicz MM, et al. (1986) The nucleotide sequence of the Escherichia coli K12 dnaJ+ gene. A gene that encodes a heat shock protein. J Biol Chem 261: 1782-1785.
65. Kostyal DA, Farrell M, McCabe A, Mei Z, Firshein W, (1989) Replication of an RK2 miniplasmid derivative in vitro by a DNA/membrane complex extracted from Escherichia coli: involvement of the dnaA but not dnaK host proteins and association of these and plasmid-encoded proteins with the inner membrane. Plasmid 21: 226-237.
66. Wickström D, Wagner S, Simonsson P, Pop O, Baars L, et al. (2011) Characterization of the consequences of YidC depletion on the inner membrane proteome of E. coli using 2D blue native/SDS-PAGE. J Mol Biol 409: 124-135 doi:10.1016/j.jmb.2011.03.068.
67. Wickstrom (2011) Consequences of depletion of the signal recognition particle in Escherichia coli. J Biol Chem 286: 4598-4609 doi:10.1074/jbc.M109.081935.
68. Lasserre J-P, Beyne E, Pyndiah S, Lapaillerie D, Claverol S, et al. (2006) A complexomic study of Escherichia coli using two-dimensional blue native/SDS polyacrylamide gel electrophoresis. Electrophoresis 27: 3306-3321 doi:10.1002/elps.200500912.
69. Mircheva M, Boy D, Weiche B, Hucke F, Graumann P, et al. (2009) Predominant membrane localization is an essential feature of the bacterial signal recognition particle receptor. BMC Biol 7: 76 doi:10.1186/1741-7007-7-76.
70. Luirink J, Hagen-Jongman ten CM, van der Weijden CC, Oudega B, High S, et al. (1994) An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J 13: 2289-2296.
71. Heinrich J, Wiegert T, (2009) Regulated intramembrane proteolysis in the control of extracytoplasmic function sigma factors. Res Microbiol 160: 696-703 doi:10.1016/j.resmic.2009.08.019.
72. Österberg S, Peso-Santos TD, Shingler V, (2011) Regulation of alternative sigma factor use. Annu Rev Microbiol 65: 37-55 doi:10.1146/annurev.micro.112408.134219.
73. Kroos L, Kunkel B, Losick R, (1989) Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science 243: 526-529.
74. Lu S, Halberg R, Kroos L, (1990) Processing of the mother-cell sigma factor, sigma K, may depend on events occurring in the forespore during Bacillus subtilis development. Proc Natl Acad Sci USA 87: 9722-9726.
75. Cutting S, Oke V, Driks A, Losick R, Lu S, et al. (1990) A forespore checkpoint for mother cell gene expression during development in B. subtilis. Cell 62: 239-250.
76. Hughes KT, Mathee K, (1998) The anti-sigma factors. Annu Rev Microbiol 52: 231-286.
77. Li X, Henry R, Yuan J, Cline K, Hoffman NE, (1995) 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: 3789-3793.
78. McLennan N, Masters M, (1998) GroE is vital for cell-wall synthesis. Nature 392: 139 doi:10.1038/32317.
79. Stark MJM, (1987) Multicopy expression vectors carrying the lac repressor gene for regulated high-level expression of genes in Escherichia coli. Gene 51: 255-267 doi:10.1016/0378-1119(87)90314-3.
80. Koo B-M, Rhodius VA, Campbell EA, Gross CA, (2009) Dissection of recognition determinants of Escherichia coli σ32 suggests a composite -10 region with an "extended -10" motif and a core -10 element. Mol Microbiol 72: 815-829 doi:10.1111/j.1365-2958.2009.06690.x.
81. Peluso P, Shan S-O, Nock S, Herschlag D, Walter P, (2001) Role of SRP RNA in the GTPase Cycles of Ffh and FtsY. Biochemistry 40: 15224-15233 doi:10.1021/bi011639y.
82. Kusters I, van den Bogaart G, Kedrov A, Krasnikov V, Fulyani F, et al. (2011) Quaternary structure of SecA in solution and bound to SecYEG probed at the single molecule level. Structure/Folding and Design 19: 430-439 doi:10.1016/j.str.2010.12.016.
83. Wu Y, Li Q, Chen X-Z, (2007) Detecting protein-protein interactions by far western blotting. Nat Protoc 2: 3278-3284 doi:10.1038/nprot.2007.459.
84. Narita S-I, Masui C, Suzuki T, Dohmae N, Akiyama Y, (2013) Protease homolog BepA (YfgC) promotes assembly and degradation of β-barrel membrane proteins in Escherichia coli. Proc Natl Acad Sci doi:10.1073/pnas.1312012110.
85. Manoil C, Beckwith J, (1985) TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci USA 82: 8129-8133.
86. Alba BM, (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma E-dependent extracytoplasmic stress response. Genes & Development 16: 2156-2168 doi:10.1101/gad.1008902.
87. Blomfield IC, Vaughn V, Rest RF, Eisenstein BI, (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5: 1447-1457.