Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 8, 2014, Pages 1442-1456

  Castanié Cornet, Marie Pierre ^a   Bruel, Nicolas ^a   Genevaux, Pierre ^a  

^a CNRS   (France)

Author keywords

DnaJ Hsp40; DnaK Hsp70; GroEL Hsp60; Protein targeting pathway; SecA SecB; Trigger factor

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; CHAPERONIN 60; GROESL PROTEIN; MEMBRANE PROTEIN; PROTEIN; PROTEIN DNAK; PROTEIN PRECURSOR; PROTEIN SECA; PROTEIN SECB; REDOX ENZYME MATURATION PROTEIN; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; TRANSACTIVATOR PROTEIN; TRIGGER FACTOR; UNCLASSIFIED DRUG;

BACTERIAL MEMBRANE; CELL ADHESION; CROSS LINKING; ESCHERICHIA COLI; LIGAND BINDING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION;

DNAJ/HSP40; DNAK/HSP70; GROEL/HSP60; PROTEIN TARGETING PATHWAY; SECA-SECB; TRIGGER FACTOR;

BACTERIA; CELL MEMBRANE; CHAPERONIN 60; HSP70 HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; OXIDATION-REDUCTION; PROTEIN TRANSPORT; SIGNAL RECOGNITION PARTICLE;

EID: 84902255537     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.11.007     Document Type: Review

References (210)

1. Fedyunin I., Lehnhardt L., Bohmer N., Kaufmann P., Zhang G., Ignatova Z. tRNA concentration fine tunes protein solubility. FEBS Lett. 2012, 586:3336-3340.
2. Bruel N., Castanie-Cornet M.P., Cirinesi A.M., Koningstein G., Georgopoulos C., Luirink J., Genevaux P. Hsp33 controls elongation factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and trigger factor chaperones. J. Biol. Chem. 2012, 287:44435-44446.
3. Komar A.A. A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 2009, 34:16-24.
4. Cortazzo P., Cervenansky C., Marin M., Reiss C., Ehrlich R., Deana A. Silent mutations affect in vivo protein folding in Escherichia coli. Biochem. Biophys. Res. Commun. 2002, 293:537-541.
5. Crombie T., Boyle J.P., Coggins J.R., Brown A.J. The folding of the bifunctional TRP3 protein in yeast is influenced by a translational pause which lies in a region of structural divergence with Escherichia coli indoleglycerol-phosphate synthase. Eur. J. Biochem. 1994, 226:657-664.
6. Lu J., Deutsch C. Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 2005, 12:1123-1129.
7. Kosolapov A., Deutsch C. Tertiary interactions within the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 2009, 16:405-411.
8. Kaiser C.M., Goldman D.H., Chodera J.D., Tinoco I., Bustamante C. The ribosome modulates nascent protein folding. Science 2011, 334:1723-1727.
9. Kramer G., Boehringer D., Ban N., Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16:589-597.
10. Sandikci A., Gloge F., Martinez M., Mayer M.P., Wade R., Bukau B., Kramer G. Dynamic enzyme docking to the ribosome coordinates N-terminal processing with polypeptide folding. Nat. Struct. Mol. Biol. 2013, 20:843-850.
11. Luirink J., Sinning I. SRP-mediated protein targeting: structure and function revisited. Biochim. Biophys. Acta 2004, 1694:17-35.
12. Dalbey R.E., Wang P., Kuhn A. Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 2011, 80:161-187.
13. Frobel J., Rose P., Muller M. Twin-arginine-dependent translocation of folded proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:1029-1046.
14. Kudva R., Denks K., Kuhn P., Vogt A., Muller M., Koch H.G. Protein translocation across the inner membrane of Gram-negative bacteria: the Sec and Tat dependent protein transport pathways. Res. Microbiol. 2013, 164:505-534.
15. Driessen A.J.M., Nouwen N. Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 2008, 77:643-667.
16. Randall L.L., Hardy S.J. SecB, one small chaperone in the complex milieu of the cell. Cell. Mol. Life Sci. 2002, 59:1617-1623.
17. Mao C., Cheadle C.E., Hardy S.J., Lilly A.A., Suo Y., Sanganna Gari R.R., King G.M., Randall L.L. Stoichiometry of SecYEG in the active translocase of Escherichia coli varies with precursor species. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11815-11820.
18. Huber D., Rajagopalan N., Preissler S., Rocco M.A., Merz F., Kramer G., Bukau B. SecA interacts with ribosomes in order to facilitate posttranslational translocation in bacteria. Mol. Cell 2011, 41:343-353.
19. Sala A., Calderon V., Bordes P., Genevaux P. TAC from Mycobacterium tuberculosis: a paradigm for stress-responsive toxin-antitoxin systems controlled by SecB-like chaperones. Cell Stress Chaperones 2013, 18:129-135.
20. Chatzi K.E., Sardis M.F., Karamanou S., Economou A. Breaking on through to the other side: protein export through the bacterial Sec system. Biochem. J. 2013, 449:25-37.
21. Palmer T., Berks B.C. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 2012, 10:483-496.
22. Robinson C., Matos C.F., Beck D., Ren C., Lawrence J., Vasisht N., Mendel S. Transport and proofreading of proteins by the twin-arginine translocation (Tat) system in bacteria. Biochim. Biophys. Acta 2011, 1808:876-884.
23. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009, 16:574-581.
24. Teter S.A., Houry W.A., Ang D., Tradler T., Rockabrand D., Fischer G., Blum P., Georgopoulos C., Hartl F.U. Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 1999, 97:755-765.
25. Deuerling E., Schulze-Specking A., Tomoyasu T., Mogk A., Bukau B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 1999, 400:693-696.
26. Agashe V.R., Guha S., Chang H.C., Genevaux P., Hayer-Hartl M., Stemp M., Georgopoulos C., Hartl F.U., Barral J.M. Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell 2004, 117:199-209.
27. Kerner M.J., Naylor D.J., Ishihama Y., Maier T., Chang H.C., Stines A.P., Georgopoulos C., Frishman D., Hayer-Hartl M., Mann M., Hartl F.U. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 2005, 122:209-220.
28. Calloni G., Chen T., Schermann S.M., Chang H.C., Genevaux P., Agostini F., Tartaglia G.G., Hayer-Hartl M., Hartl F.U. DnaK functions as a central hub in the E. coli chaperone network. Cell Rep. 2012, 1:251-264.
29. Valent Q.A., Kendall D.A., High S., Kusters R., Oudega B., Luirink J. Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 1995, 14:5494-5505.
30. Ferbitz L., Maier T., Patzelt H., Bukau B., Deuerling E., Ban N. Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 2004, 431:590-596.
31. Genevaux P., Keppel F., Schwager F., Langendijk-Genevaux P.S., Hartl F.U., Georgopoulos C. In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep. 2004, 5:195-200.
32. Kramer G., Rauch T., Rist W., Vorderwulbecke S., Patzelt H., Schulze-Specking A., Ban N., Deuerling E., Bukau B. L23 protein functions as a chaperone docking site on the ribosome. Nature 2002, 419:171-174.
33. Lakshmipathy S.K., Tomic S., Kaiser C.M., Chang H.C., Genevaux P., Georgopoulos C., Barral J.M., Johnson A.E., Hartl F.U., Etchells S.A. Identification of nascent chain interaction sites on trigger factor. J. Biol. Chem. 2007, 282:12186-12193.
34. Merz F., Hoffmann A., Rutkowska A., Zachmann-Brand B., Bukau B., Deuerling E. The C-terminal domain of Escherichia coli trigger factor represents the central module of its chaperone activity. J. Biol. Chem. 2006, 281:31963-31971.
35. Hoffmann A., Bukau B., Kramer G. Structure and function of the molecular chaperone Trigger Factor. Biochim. Biophys. Acta, Mol. Cell. Res. 2010, 1803:650-661.
36. Kristensen O., Gajhede M. Chaperone binding at the ribosomal exit tunnel. Structure (Camb) 2003, 11:1547-1556.
37. Maillard J., Genevaux P., Holliger C. Redundancy and specificity of multiple trigger factor chaperones in Desulfitobacteria. Microbiology 2011, 157:2410-2421.
38. Raine A., Lovmar M., Wikberg J., Ehrenberg M. Trigger factor binding to ribosomes with nascent peptide chains of varying lengths and sequences. J. Biol. Chem. 2013, 281:28033-28038.
39. Crooke E., Guthrie B., Lecker S., Lill R., Wickner W. ProOmpA is stabilized for membrane translocation by either purified E. coli trigger factor or canine signal recognition particle. Cell 1988, 54:1003-1011.
40. Kaiser C.M., Chang H.C., Agashe V.R., Lakshmipathy S.K., Etchells S.A., Hayer-Hartl M., Hartl F.U., Barral J.M. Real-time observation of trigger factor function on translating ribosomes. Nature 2006, 444:455-460.
41. Martinez-Hackert E., Hendrickson W.A. Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell 2009, 138:923-934.
42. Merz F., Boehringer D., Schaffitzel C., Preissler S., Hoffmann A., Maier T., Rutkowska A., Lozza J., Ban N., Bukau B., Deuerling E. Molecular mechanism and structure of Trigger Factor bound to the translating ribosome. EMBO J. 2008, 27:1622-1632.
43. Houben E.N., Zarivach R., Oudega B., Luirink J. Early encounters of a nascent membrane protein: specificity and timing of contacts inside and outside the ribosome. J. Cell Biol. 2005, 170:27-35.
44. Oh E., Becker A.H., Sandikci A., Huber D., Chaba R., Gloge F., Nichols R.J., Typas A., Gross C.A., Kramer G., Weissman J.S., Bukau B. Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 2011, 147:1295-1308.
45. Ball L.A., Kaesberg P. Cleavage of the N-terminal formylmethionine residue from a bacteriophage coat protein in vitro. J. Mol. Biol. 1973, 79:531-537.
46. Bingel-Erlenmeyer R., Kohler R., Kramer G., Sandikci A., Antolic S., Maier T., Schaffitzel C., Wiedmann B., Bukau B., Ban N. A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing. Nature 2008, 452:108-U113.
47. Keenan R.J., Freymann D.M., Stroud R.M., Walter P. The signal recognition particle. Annu. Rev. Biochem. 2001, 70:755-775.
48. Patzelt H., Rudiger S., Brehmer D., Kramer G., Vorderwulbecke S., Schaffitzel E., Waitz A., Hesterkamp T., Dong L., Schneider-Mergener J., Bukau B., Deuerling E. Binding specificity of Escherichia coli trigger factor. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:14244-14249.
49. Lakshmipathy S.K., Gupta R., Pinkert S., Etchells S.A., Hartl F.U. Versatility of trigger factor interactions with ribosome-nascent chain complexes. J. Biol. Chem. 2010, 285:27911-27923.
50. Hoffmann A., Merz F., Rutkowska A., Zachmann-Brand B., Deuerling E., Bukau B. Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J. Biol. Chem. 2006, 281:6539-6545.
51. Hoffmann A., Becker A.H., Zachmann-Brand B., Deuerling E., Bukau B., Kramer G. Concerted action of the ribosome and the associated chaperone trigger factor confines nascent polypeptide folding. Mol. Cell 2012, 48:63-74.
52. O'Brien E.P., Christodoulou J., Vendruscolo M., Dobson C.M. Trigger factor slows co-translational folding through kinetic trapping while sterically protecting the nascent chain from aberrant cytosolic interactions. J. Am. Chem. Soc. 2012, 134:10920-10932.
53. Guthrie B., Wickner W. Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol. 1990, 172:5555-5562.
54. Kandror O., Goldberg A.L. Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4978-4981.
55. Nichols R.J., Sen S., Choo Y.J., Beltrao P., Zietek M., Chaba R., Lee S., Kazmierczak K.M., Lee K.J., Wong A., Shales M., Lovett S., Winkler M.E., Krogan N.J., Typas A., Gross C.A. Phenotypic landscape of a bacterial cell. Cell 2011, 144:143-156.
56. Reyes D.Y., Yoshikawa H. DnaK chaperone machine and trigger factor are only partially required for normal growth of Bacillus subtilis. Biosci. Biotechnol. Biochem. 2002, 66:1583-1586.
57. Gothel S.F., Scholz C., Schmid F.X., Marahiel M.A. Cyclophilin and trigger factor from Bacillus subtilis catalyze in vitro protein folding and are necessary for viability under starvation conditions. Biochemistry 1998, 37:13392-13399.
58. Miller-Williams M., Loewen P.C., Oresnik I.J. Isolation of salt-sensitive mutants of Sinorhizobium meliloti strain Rm1021. Microbiology 2006, 152:2049-2059.
59. Bigot A., Botton E., Dubail I., Charbit A. A homolog of Bacillus subtilis trigger factor in Listeria monocytogenes is involved in stress tolerance and bacterial virulence. Appl. Environ. Microbiol. 2006, 72:6623-6631.
60. Crowley P.J., Seifert T.B., Isoda R., van Tilburg M., Oli M.W., Robinette R.A., McArthur W.P., Bleiweis A.S., Brady L.J. Requirements for surface expression and function of adhesin P1 from Streptococcus mutans. Infect. Immun. 2008, 76:2456-2468.
61. Wen Z.T., Suntharaligham P., Cvitkovitch D.G., Burne R.A. Trigger factor in Streptococcus mutans is involved in stress tolerance, competence development, and biofilm formation. Infect. Immun. 2005, 73:219-225.
62. Lyon W.R., Gibson C.M., Caparon M.G. A role for trigger factor and an rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J. 1998, 17:6263-6275.
63. Genevaux P., Georgopoulos C., Kelley W.L. The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol. Microbiol. 2007, 66:840-857.
64. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
65. Swain J.F., Dinler G., Sivendran R., Montgomery D.L., Stotz M., Gierasch L.M. Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 2007, 26:27-39.
66. Vogel M., Mayer M.P., Bukau B. Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker. J. Biol. Chem. 2006, 281:38705-38711.
67. Smock R.G., Blackburn M.E., Gierasch L.M. Conserved, disordered C terminus of DnaK enhances cellular survival upon stress and DnaK in vitro chaperone activity. J. Biol. Chem. 2011, 286:31821-31829.
68. Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:2874-2878.
69. Harrison C.J., Hayer-Hartl M., Di Liberto M., Hartl F., Kuriyan J. Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 1997, 276:431-435.
70. Brehmer D., Rudiger S., Gassler C.S., Klostermeier D., Packschies L., Reinstein J., Mayer M.P., Bukau B. Tuning of chaperone activity of Hsp70 proteins by modulation of nucleotide exchange. Nat. Struct. Biol. 2001, 8:427-432.
71. Rudiger S., Germeroth L., Schneider-Mergener J., Bukau B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 1997, 16:1501-1507.
72. Tartaglia G.G., Dobson C.M., Hartl F.U., Vendruscolo M. Physicochemical determinants of chaperone requirements. J. Mol. Biol. 2010, 400:579-588.
73. Mogk A., Huber D., Bukau B. Integrating protein homeostasis strategies in prokaryotes. Cold Spring Harb. Perspect. Biol. 2011, 3.
74. Bukau B., Walker G.C. Delta dnaK52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures. J. Bacteriol. 1989, 171:6030-6038.
75. Lemos J.A., Luzardo Y., Burne R.A. Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J. Bacteriol. 2007, 189:1582-1588.
76. Griffin J.E., Gawronski J.D., Dejesus M.A., Ioerger T.R., Akerley B.J., Sassetti C.M. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog. 2011, 7:e1002251.
77. Schulz A., Tzschaschel B., Schumann W. Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol. Microbiol. 1995, 15:421-429.
78. Selby K., Lindstrom M., Somervuo P., Heap J.T., Minton N.P., Korkeala H. Important role of class I heat shock genes hrcA and dnaK in the heat shock response and the response to pH and NaCl stress of group I Clostridium botulinum strain ATCC 3502. Appl. Environ. Microbiol. 2011, 77:2823-2830.
79. Chakrabarti S., Sengupta N., Chowdhury R. Role of DnaK in in vitro and in vivo expression of virulence factors of Vibrio cholerae. Infect. Immun. 1999, 67:1025-1033.
80. Tomoyasu T., Tabata A., Imaki H., Tsuruno K., Miyazaki A., Sonomoto K., Whiley R.A., Nagamune H. Role of Streptococcus intermedius DnaK chaperone system in stress tolerance and pathogenicity. Cell Stress Chaperones 2012, 17:41-55.
81. Takaya A., Tomoyasu T., Matsui H., Yamamoto T. The DnaK/DnaJ chaperone machinery of Salmonella enterica serovar Typhimurium is essential for invasion of epithelial cells and survival within macrophages, leading to systemic infection. Infect. Immun. 2004, 72:1364-1373.
82. Kohler S., Ekaza E., Paquet J.Y., Walravens K., Teyssier J., Godfroid J., Liautard J.P. Induction of dnaK through its native heat shock promoter is necessary for intramacrophagic replication of Brucella suis. Infect. Immun. 2002, 70:1631-1634.
83. Hanawa T., Fukuda M., Kawakami H., Hirano H., Kamiya S., Yamamoto T. The Listeria monocytogenes DnaK chaperone is required for stress tolerance and efficient phagocytosis with macrophages. Cell Stress Chaperones 1999, 4:118-128.
84. Singh V.K., Utaida S., Jackson L.S., Jayaswal R.K., Wilkinson B.J., Chamberlain N.R. Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus. Microbiology 2007, 153:3162-3173.
85. Saibil H.R., Fenton W.A., Clare D.K., Horwich A.L. Structure and allostery of the chaperonin GroEL. J. Mol. Biol. 2013, 425:1476-1487.
86. Shewmaker F., Maskos K., Simmerling C., Landry S.J. The disordered mobile loop of GroES folds into a defined beta-hairpin upon binding GroEL. J. Biol. Chem. 2001, 276:31257-31264.
87. Nojima T., Ikegami T., Taguchi H., Yoshida M. Flexibility of GroES mobile loop is required for efficient chaperonin function. J. Mol. Biol. 2012, 422:291-299.
88. Jewett A.I., Shea J.E. Reconciling theories of chaperonin accelerated folding with experimental evidence. Cell. Mol. Life Sci. 2010, 67:255-276.
89. Horwich A.L., Fenton W.A. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q. Rev. Biophys. 2009, 42:83-116.
90. Tang Y.C., Chang H.C., Roeben A., Wischnewski D., Wischnewski N., Kerner M.J., Hartl F.U., Hayer-Hartl M. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 2006, 125:903-914.
91. Lin Z., Madan D., Rye H.S. GroEL stimulates protein folding through forced unfolding. Nat. Struct. Mol. Biol. 2008, 15:303-311.
92. Fujiwara K., Ishihama Y., Nakahigashi K., Soga T., Taguchi H. A systematic survey of in vivo obligate chaperonin-dependent substrates. EMBO J. 2010, 29:1552-1564.
93. Fayet O., Ziegelhoffer T., Georgopoulos C. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol. 1989, 171:1379-1385.
94. Niwa T., Ying B.W., Saito K., Jin W., Takada S., Ueda T., Taguchi H. Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4201-4206.
95. Chapman E., Farr G.W., Usaite R., Furtak K., Fenton W.A., Chaudhuri T.K., Hondorp E.R., Matthews R.G., Wolf S.G., Yates J.R., Pypaert M., Horwich A.L. Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15800-15805.
96. Arifuzzaman M., Maeda M., Itoh A., Nishikata K., Takita C., Saito R., Ara T., Nakahigashi K., Huang H.C., Hirai A., Tsuzuki K., Nakamura S., Altaf-Ul-Amin M., Oshima T., Baba T., Yamamoto N., Kawamura T., Ioka-Nakamichi T., Kitagawa M., Tomita M., Kanaya S., Wada C., Mori H. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 2006, 16:686-691.
97. Priya S., Sharma S.K., Sood V., Mattoo R.U., Finka A., Azem A., De Los Rios P., Goloubinoff P. GroEL and CCT are catalytic unfoldases mediating out-of-cage polypeptide refolding without ATP. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7199-7204.
98. Georgopoulos C.P., Eisen H. Bacterial mutants which block phage assembly. J. Supramol. Struct. 1974, 2:349-359.
99. Horwich A.L., Low K.B., Fenton W.A., Hirshfield I.N., Furtak K. Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 1993, 74:909-917.
100. Kanemori M., Mori H., Yura T. Effects of reduced levels of GroE chaperones on protein metabolism: enhanced synthesis of heat shock proteins during steady-state growth of Escherichia coli. J. Bacteriol. 1994, 176:4235-4242.
101. McLennan N., Masters M. GroE is vital for cell-wall synthesis. Nature 1998, 392:139.
102. Li M., Wong S.L. Cloning and characterization of the groESL operon from Bacillus subtilis. J. Bacteriol. 1992, 174:3981-3992.
103. Nasrallah G.K., Gagnon E., Orton D.J., Garduno R.A. The htpAB operon of Legionella pneumophila cannot be deleted in the presence of the groE chaperonin operon of Escherichia coli. Can. J. Microbiol. 2011, 57:943-952.
104. Susin M.F., Baldini R.L., Gueiros-Filho F., Gomes S.L. GroES/GroEL and DnaK/DnaJ have distinct roles in stress responses and during cell cycle progression in Caulobacter crescentus. J. Bacteriol. 2006, 188:8044-8053.
105. Lund P.A. Multiple chaperonins in bacteria-why so many?. FEMS Microbiol. Rev. 2009, 33:785-800.
106. Bittner A.N., Foltz A., Oke V. Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti. J. Bacteriol. 2007, 189:1884-1889.
107. Li J., Wang Y., Zhang C.Y., Zhang W.Y., Jiang D.M., Wu Z.H., Liu H., Li Y.Z. Myxococcus xanthus viability depends on groEL supplied by either of two genes, but the paralogs have different functions during heat shock, predation, and development. J. Bacteriol. 2010, 192:1875-1881.
108. Rodriguez-Quinones F., Maguire M., Wallington E.J., Gould P.S., Yerko V., Downie J.A., Lund P.A. Two of the three groEL homologues in Rhizobium leguminosarum are dispensable for normal growth. Arch. Microbiol. 2005, 183:253-265.
109. Lee W.T., Terlesky K.C., Tabita F.R. Cloning and characterization of two groESL operons of Rhodobacter sphaeroides: transcriptional regulation of the heat-induced groESL operon. J. Bacteriol. 1997, 179:487-495.
110. Sato M., Nimura-Matsune K., Watanabe S., Chibazakura T., Yoshikawa H. Expression analysis of multiple dnaK genes in the cyanobacterium Synechococcus elongatus PCC 7942. J. Bacteriol. 2007, 189:3751-3758.
111. Ojha A., Anand M., Bhatt A., Kremer L., Jacobs W.R., Hatfull G.F. GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 2005, 123:861-873.
112. Hu Y., Henderson B., Lund P.A., Tormay P., Ahmed M.T., Gurcha S.S., Besra G.S., Coates A.R. A Mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable but fails to induce an inflammatory response in animal models of infection. Infect. Immun. 2008, 76:1535-1546.
113. Glass J.I., Lefkowitz E.J., Glass J.S., Heiner C.R., Chen E.Y., Cassell G.H. The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature 2000, 407:757-762.
114. Barre A., de Daruvar A., Blanchard A. MolliGen, a database dedicated to the comparative genomics of Mollicutes. Nucleic Acids Res. 2004, 32:D307-310.
115. Hutchison C.A., Peterson S.N., Gill S.R., Cline R.T., White O., Fraser C.M., Smith H.O., Venter J.C. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 1999, 286:2165-2169.
116. Clark G.W., Tillier E.R. Loss and gain of GroEL in the Mollicutes. Biochem. Cell Biol. 2010, 88:185-194.
117. Vorderwulbecke S., Kramer G., Merz F., Kurz T.A., Rauch T., Zachmann-Brand B., Bukau B., Deuerling E. Low temperature or GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. FEBS Lett. 2004, 559:181-187.
118. Ullers R.S., Luirink J., Harms N., Schwager F., Georgopoulos C., Genevaux P. SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7583-7588.
119. Bordes P., Cirinesi A.M., Ummels R., Sala A., Sakr S., Bitter W., Genevaux P. SecB-like chaperone controls a toxin-antitoxin stress-responsive system in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8438-8443.
120. Crooke E., Wickner W. Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:5216-5220.
121. Crooke E., Brundage L., Rice M., Wickner W. ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes. EMBO J. 1988, 7:1831-1835.
122. Lecker S., Lill R., Ziegelhoffer T., Georgopoulos C., Bassford P.J., Kumamoto C.A., Wickner W. Three pure chaperone proteins of Escherichia coli-SecB, trigger factor and GroEL-form soluble complexes with precursor proteins in vitro. EMBO J. 1989, 8:2703-2709.
123. Lee H.C., Bernstein H.D. Trigger factor retards protein export in E. coli. J. Biol. Chem. 2002, 29:29.
124. Lill R., Crooke E., Guthrie B., Wickner W. The "trigger factor cycle" includes ribosomes, presecretory proteins, and the plasma membrane. Cell 1988, 54:1013-1018.
125. Ullers R.S., Ang D., Schwager F., Georgopoulos C., Genevaux P. Trigger Factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3101-3106.
126. Ricci D.P., Silhavy T.J. The Bam machine: a molecular cooper. Biochim. Biophys. Acta 2012, 1818:1067-1084.
127. Gouridis G., Karamanou S., Gelis I., Kalodimos C.G., Economou A. Signal peptides are allosteric activators of the protein translocase. Nature 2009, 462:363-367.
128. Kadokura H., Beckwith J. Detecting folding intermediates of a protein as it passes through the bacterial translocation channel. Cell 2009, 138:1164-1173.
129. Josefsson L.G., Randall L.L. Different exported proteins in E. coli show differences in the temporal mode of processing in vivo. Cell 1981, 25:151-157.
130. Bornemann T., Jockel J., Rodnina M.V., Wintermeyer W. Signal sequence-independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nat. Struct. Mol. Biol. 2008, 15:494-499.
131. Lin K.F., Sun C.S., Huang Y.C., Chan S.I., Koubek J., Wu T.H., Huang J.J. Cotranslational protein folding within the ribosome tunnel influences trigger-factor recruitment. Biophys. J. 2012, 102:2818-2827.
132. Eisner G., Koch H.G., Beck K., Brunner J., Muller M. Ligand crowding at a nascent signal sequence. J. Cell Biol. 2003, 163:35-44.
133. Beck K., Wu L.F., Brunner J., Muller M. Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 2000, 19:134-143.
134. Ullers R.S., Houben E.N., Raine A., ten Hagen-Jongman C.M., Ehrenberg M., Brunner J., Oudega B., Harms N., Luirink J. Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J. Cell Biol. 2003, 161:679-684.
135. Ullers R.S., Houben E.N., Brunner J., Oudega B., Harms N., Luirink J. Sequence-specific interactions of nascent Escherichia coli polypeptides with trigger factor and signal recognition particle. J. Biol. Chem. 2006, 281:13999-14005.
136. Lee H.C., Bernstein H.D. The targeting pathway of Escherichia coli presecretory and integral membrane proteins is specified by the hydrophobicity of the targeting signal. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3471-3476.
137. Karamyshev A.L., Johnson A.E. 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. 2005, 280:37930-37940.
138. Jong W.S., Hagen-Jongman C.M., Genevaux P., Brunner J., Oudega B., Luirink J. Trigger factor interacts with the signal peptide of nascent Tat substrates but does not play a critical role in Tat-mediated export. Eur. J. Biochem. 2004, 271:4779-4787.
139. Morita Y., Futagami T., Goto M., Furukawa K. Functional characterization of the trigger factor protein PceT of tetrachloroethene-dechlorinating Desulfitobacterium hafniense Y51. Appl. Microbiol. Biotechnol. 2009, 83:775-781.
140. Lyon W.R., Caparon M.G. Trigger factor-mediated prolyl isomerization influences maturation of the Streptococcus pyogenes cysteine protease. J. Bacteriol. 2003, 185:3661-3667.
141. Phillips G.J., Silhavy T.J. Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature 1990, 344:882-884.
142. Wild J., Walter W.A., Gross C.A., Altman E. Accumulation of secretory protein precursors in Escherichia coli induces the heat shock response. J. Bacteriol. 1993, 175:3992-3997.
143. Ito K., Akiyama Y., Yura T., Shiba K. Diverse effects of the MalE-LacZ hybrid protein on Escherichia coli cell physiology. J. Bacteriol. 1986, 167:201-204.
144. Altman E., Kumamoto C.A., Emr S.D. Heat-shock proteins can substitute for SecB function during protein export in Escherichia coli. EMBO J. 1991, 10:239-245.
145. Wild J., Altman E., Yura T., Gross C.A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 1992, 6:1165-1172.
146. Moran-Barrio J., Limansky A.S., Viale A.M. Secretion of GOB metallo-beta-lactamase in Escherichia coli depends strictly on the cooperation between the cytoplasmic DnaK chaperone system and the Sec machinery: completion of folding and Zn(II) ion acquisition occur in the bacterial periplasm. Antimicrob. Agents Chemother. 2009, 53:2908-2917.
147. Qi H.Y., Hyndman J.B., Bernstein H.D. DnaK promotes the selective export of outer membrane protein precursors in SecA-deficient Escherichia coli. J. Biol. Chem. 2002, 277:51077-51083.
148. Muller J.P. Influence of impaired chaperone or secretion function on SecB production in Escherichia coli. J. Bacteriol. 1996, 178:6097-6104.
149. Sakr S., Cirinesi A.M., Ullers R.S., Schwager F., Georgopoulos C., Genevaux P. Lon protease quality control of presecretory proteins in Escherichia coli and its dependence on the SecB and DnaJ (Hsp40) chaperones. J. Biol. Chem. 2010, 285:23504-23512.
150. Dautin N., Bernstein H.D. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 2007, 61:89-112.
151. Grijpstra J., Arenas J., Rutten L., Tommassen J. Autotransporter secretion: varying on a theme. Res. Microbiol. 2013, 164:562-582.
152. Jong W.S., ten Hagen-Jongman C.M., Ruijter E., Orru R.V., Genevaux P., Luirink J. YidC is involved in the biogenesis of the secreted autotransporter hemoglobin protease. J. Biol. Chem. 2010, 285:39682-39690.
153. Jiang X., Ruiz T., Mintz K.P. Characterization of the secretion pathway of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans. Mol. Oral Microbiol. 2012, 27:382-396.
154. Janakiraman A., Fixen K.R., Gray A.N., Niki H., Goldberg M.B. A genome-scale proteomic screen identifies a role for DnaK in chaperoning of polar autotransporters in Shigella. J. Bacteriol. 2009, 191:6300-6311.
155. Bukau B., Reilly P., McCarty J., Walker G.C. Immunogold localization of the DnaK heat shock protein in Escherichia coli cells. J. Gen. Microbiol. 1993, 139:95-99.
156. Klepsch M., Schlegel S., Wickstrom D., Friso G., van Wijk K.J., Persson J.O., de Gier J.W., Wagner S. Immobilization of the first dimension in 2D blue native/SDS-PAGE allows the relative quantification of membrane proteomes. Methods 2008, 46:48-53.
157. Stenberg F., Chovanec P., Maslen S.L., Robinson C.V., Ilag L.L., von Heijne G., Daley D.O. Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 2005, 280:34409-34419.
158. Wickstrom D., Wagner S., Baars L., Ytterberg A.J., Klepsch M., van Wijk K.J., Luirink J., de Gier J.W. Consequences of depletion of the signal recognition particle in Escherichia coli. J. Biol. Chem. 2011, 286:4598-4609.
159. Bernstein H.D., Hyndman J.B. Physiological basis for conservation of the signal recognition particle targeting pathway in Escherichia coli. J. Bacteriol. 2001, 183:2187-2197.
160. Wickstrom D., Wagner S., Simonsson P., Pop O., Baars L., Ytterberg A.J., van Wijk K.J., Luirink J., de Gier J.W. Characterization of the consequences of YidC depletion on the inner membrane proteome of E. coli using 2D blue native/SDS-PAGE. J. Mol. Biol. 2011, 409:124-135.
161. Borgese N., Fasana E. Targeting pathways of C-tail-anchored proteins. Biochim. Biophys. Acta 2011, 1808:937-946.
162. Aschtgen M.S., Zoued A., Lloubes R., Journet L., Cascales E. The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC. Microbiologyopen 2012, 1:71-82.
163. Clarke D.J., Jacq A., Holland I.B. A novel DnaJ-like protein in Escherichia coli inserts into the cytoplasmic membrane with a type III topology. Mol. Microbiol. 1996, 20:1273-1286.
164. Kelley W.L., Georgopoulos C. Positive control of the two-component RcsC/B signal transduction network by DjlA: a member of the DnaJ family of molecular chaperones in Escherichia coli. Mol. Microbiol. 1997, 25:913-931.
165. Toutain C.M., Clarke D.J., Leeds J.A., Kuhn J., Beckwith J., Holland I.B., Jacq A. The transmembrane domain of the DnaJ-like protein DjlA is a dimerisation domain. Mol. Genet. Genomics 2003, 268:761-770.
166. Genevaux P., Wawrzynow A., Zylicz M., Georgopoulos C., Kelley W.L. DjlA is a third DnaK co-chaperone of Escherichia coli, and DjlA-mediated induction of colanic acid capsule requires DjlA-DnaK interaction. J. Biol. Chem. 2001, 276:7906-7912.
167. Genevaux P., Schwager F., Georgopoulos C., Kelley W.L. The djlA gene acts synergistically with dnaJ in promoting Escherichia coli growth. J. Bacteriol. 2001, 183:5747-5750.
168. Vincent C.D., Buscher B.A., Friedman J.R., Williams L.A., Bardill P., Vogel J.P. Identification of non-dot/icm suppressors of the Legionella pneumophila DeltadotL lethality phenotype. J. Bacteriol. 2006, 188:8231-8243.
169. Ohnishi H., Mizunoe Y., Takade A., Tanaka Y., Miyamoto H., Harada M., Yoshida S. Legionella dumoffii DjlA, a member of the DnaJ family, is required for intracellular growth. Infect. Immun. 2004, 72:3592-3603.
170. Lakhal F., Bury-Mone S., Nomane Y., Le Goic N., Paillard C., Jacq A. DjlA, a membrane-anchored DnaJ-like protein, is required for cytotoxicity of clam pathogen Vibrio tapetis to hemocytes. Appl. Environ. Microbiol. 2008, 74:5750-5758.
171. Cloward J.M., Krause D.C. Mycoplasma pneumoniae J-domain protein required for terminal organelle function. Mol. Microbiol. 2009, 71:1296-1307.
172. Graubner W., Schierhorn A., Bruser T. DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J. Biol. Chem. 2007, 282:7116-7124.
173. Perez-Rodriguez R., Fisher A.C., Perlmutter J.D., Hicks M.G., Chanal A., Santini C.L., Wu L.F., Palmer T., DeLisa M.P. An essential role for the DnaK molecular chaperone in stabilizing over-expressed substrate proteins of the bacterial twin-arginine translocation pathway. J. Mol. Biol. 2007, 367:715-730.
174. Oresnik I.J., Ladner C.L., Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 2001, 40:323-331.
175. Li H., Chang L., Howell J.M., Turner R.J. DmsD, a Tat system specific chaperone, interacts with other general chaperones and proteins involved in the molybdenum cofactor biosynthesis. Biochim. Biophys. Acta 2010, 1804:1301-1309.
176. Bruser T., Yano T., Brune D.C., Daldal F. Membrane targeting of a folded and cofactor-containing protein. Eur. J. Biochem. 2003, 270:1211-1221.
177. Lecker S., Lill R., Ziegelhoffer T., Georgopoulos C., Bassford P.J., Kumamoto C.A., Wickner W. 3 pure chaperone proteins of Escherichia coli-SecB, trigger factor and Groel-form soluble complexes with precursor proteins invitro. EMBO J. 1989, 8:2703-2709.
178. Kusukawa N., Yura T., Ueguchi C., Akiyama Y., Ito K. Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J. 1989, 8:3517-3521.
179. Watanabe T., Hayashi S., Wu H.C. Synthesis and export of the outer membrane lipoprotein in Escherichia coli mutants defective in generalized protein export. J. Bacteriol. 1988, 170:4001-4007.
180. Baars L., Ytterberg A.J., Drew D., Wagner S., Thilo C., Van Wijk K.J., de Gier J.W. Defining the role of the Escherichia coli chaperone SecB using comparative proteomics. J. Biol. Chem. 2006, 281:10024-10034.
181. Van Dyk T.K., Gatenby A.A., LaRossa R.A. Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature 1989, 342:451-453.
182. Danese P.N., Murphy C.K., Silhavy T.J. Multicopy suppression of cold-sensitive sec mutations in Escherichia coli. J. Bacteriol. 1995, 177:4969-4973.
183. Bochkareva E.S., Solovieva M.E., Girshovich A.S. Targeting of GroEL to SecA on the cytoplasmic membrane of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:478-483.
184. Baars L., Wagner S., Wickstrom D., Klepsch M., Ytterberg A.J., van Wijk K.J., de Gier J.W. Effects of SecE depletion on the inner and outer membrane proteomes of Escherichia coli. J. Bacteriol. 2008, 190:3505-3525.
185. Seydlova G., Halada P., Fiser R., Toman O., Ulrych A., Svobodova J. DnaK and GroEL chaperones are recruited to the Bacillus subtilis membrane after short-term ethanol stress. J. Appl. Microbiol. 2012, 112:765-774.
186. Sharma S., Chakraborty K., Muller B.K., Astola N., Tang Y.C., Lamb D.C., Hayer-Hartl M., Hartl F.U. Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 2008, 133:142-153.
187. Laminet A.A., Ziegelhoffer T., Georgopoulos C., Pluckthun A. The Escherichia coli heat shock proteins GroEL and GroES modulate the folding of the beta-lactamase precursor. EMBO J. 1990, 9:2315-2319.
188. Rodrigue A., Batia N., Muller M., Fayet O., Bohm R., Mandrand-Berthelot M.A., Wu L.F. Involvement of the GroE chaperonins in the nickel-dependent anaerobic biosynthesis of NiFe-hydrogenases of Escherichia coli. J. Bacteriol. 1996, 178:4453-4460.
189. Hatzixanthis K., Palmer T., Sargent F. A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 2003, 49:1377-1390.
190. Kang D.G., Kim C.S., Seo J.H., Kim I.G., Choi S.S., Ha J.H., Nam S.W., Lim G., Cha H.J. Coexpression of molecular chaperone enhances activity and export of organophosphorus hydrolase in Escherichia coli. Biotechnol. Prog. 2012, 28:925-930.
191. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B., Krogan N., Davey M., Parkinson J., Greenblatt J., Emili A. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433:531-537.
192. Knaust A., Weber M.V., Hammerschmidt S., Bergmann S., Frosch M., Kurzai O. Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J. Bacteriol. 2007, 189:3246-3255.
193. Yang C.K., Ewis H.E., Zhang X., Lu C.D., Hu H.J., Pan Y., Abdelal A.T., Tai P.C. Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis. J. Bacteriol. 2011, 193:5607-5615.
194. Henderson B., Fares M.A., Lund P.A. Chaperonin 60: a paradoxical, evolutionarily conserved protein family with multiple moonlighting functions. Biol. Rev. Camb. Philos. Soc. 2013, 88:955-987.
195. Hickey T.B., Ziltener H.J., Speert D.P., Stokes R.W. Mycobacterium tuberculosis employs Cpn60.2 as an adhesin that binds CD43 on the macrophage surface. Cell. Microbiol. 2010, 12:1634-1647.
196. Yoshida N., Oeda K., Watanabe E., Mikami T., Fukita Y., Nishimura K., Komai K., Matsuda K. Protein function. Chaperonin turned insect toxin. Nature 2001, 411:44.
197. Joshi M.C., Sharma A., Kant S., Birah A., Gupta G.P., Khan S.R., Bhatnagar R., Banerjee N. An insecticidal GroEL protein with chitin binding activity from Xenorhabdus nematophila. J. Biol. Chem. 2008, 283:28287-28296.
198. Nakano H., Yamada Y., Ishikura H., Inokuchi H. A mutation in the gene for trigger factor suppresses the defect in cell division in the divE42 mutant of Escherichia coli K12. Mol. Gen. Genet. 1998, 260:75-80.
199. Hansen S., Lewis K., Vulic M. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 2008, 52:2718-2726.
200. Spence J., Cegielska A., Georgopoulos C. Role of Escherichia coli heat shock proteins DnaK and HtpG (C62.5) in response to nutritional deprivation. J. Bacteriol. 1990, 172:7157-7166.
201. Guisbert E., Herman C., Lu C.Z., Gross C.A. A chaperone network controls the heat shock response in E. coli. Genes Dev. 2004, 18:2812-2821.
202. Ang D., Georgopoulos C. The heat-shock-regulated grpE gene of Escherichia coli is required for bacterial growth at all temperatures but is dispensable in certain mutant backgrounds. J. Bacteriol. 1989, 171:2748-2755.
203. Fares M.A., Ruiz-Gonzalez M.X., Moya A., Elena S.F., Barrio E. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 2002, 417:398.
204. Wada M., Itikawa H. Participation of Escherichia coli K-12 groE gene products in the synthesis of cellular DNA and RNA. J. Bacteriol. 1984, 157:694-696.
205. Donnelly C.E., Walker G.C. groE mutants of Escherichia coli are defective in umuDC-dependent UV mutagenesis. J. Bacteriol. 1989, 171:6117-6125.
206. Yamaguchi Y., Tomoyasu T., Takaya A., Morioka M., Yamamoto T. Effects of disruption of heat shock genes on susceptibility of Escherichia coli to fluoroquinolones. BMC Microbiol. 2003, 3:16.
207. Zeilstra-Ryalls J., Fayet O., Baird L., Georgopoulos C. Sequence analysis and phenotypic characterization of groEL mutations that block lambda and T4 bacteriophage growth. J. Bacteriol. 1993, 175:1134-1143.
208. Burnett B.P., Horwich A.L., Low K.B. A carboxy-terminal deletion impairs the assembly of GroEL and confers a pleiotropic phenotype in Escherichia coli K-12. J. Bacteriol. 1994, 176:6980-6985.
209. Goltermann L., Good L., Bentin T. Chaperonins fight aminoglycoside-induced protein misfolding and promote short-term tolerance in Escherichia coli. J. Biol. Chem. 2013, 288:10483-10489.
210. Rudolph B., Gebendorfer K.M., Buchner J., Winter J. Evolution of Escherichia coli for growth at high temperatures. J. Biol. Chem. 2010, 285:19029-19034.