DnaK Functions as a Central Hub in the E. coli Chaperone Network

Cell Reports

Volumn 1, Issue 3, 2012, Pages 251-264

  Calloni, Giulia ^a   Chen, Taotao ^a   Schermann, Sonya M ^a,d   Chang, Hung Chun ^a,e   Genevaux, Pierre ^b   Agostini, Federico ^c   Tartaglia, Gian Gaetano ^c   Hayer Hartl, Manajit ^a   Hartl, F Ulrich ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b CNRS   (France)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d MICROMET AG   (Germany)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHAPERONIN; PROTEIN DNAK; TRIGGER FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; HSP70 HEAT-SHOCK PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPS; PROTEOME; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 84861139210     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2011.12.007     Document Type: Article

References (48)

1. 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.
2. Balch W.E., Morimoto R.I., Dillin A., Kelly J.W. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
3. Bitto E., McKay D.B. Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 2002, 10:1489-1498.
4. Bukau B., Walker G.C. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J. Bacteriol. 1989, 171:2337-2346.
5. 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., et al. Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL. Proc. Natl. Acad. Sci. USA 2006, 103:15800-15805.
6. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
7. 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.
8. Deuerling E., Patzelt H., Vorderwülbecke S., Rauch T., Kramer G., Schaffitzel E., Mogk A., Schulze-Specking A., Langen H., Bukau B. Trigger Factor and DnaK possess overlapping substrate pools and binding specificities. Mol. Microbiol. 2003, 47:1317-1328.
9. 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.
10. Ewalt K.L., Hendrick J.P., Houry W.A., Hartl F.U. In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 1997, 90:491-500.
11. 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.
12. 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.
13. Gamer J., Bujard H., Bukau B. Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor sigma 32. Cell 1992, 69:833-842.
14. 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.
15. Gerdes S.Y., Scholle M.D., Campbell J.W., Balázsi G., Ravasz E., Daugherty M.D., Somera A.L., Kyrpides N.C., Anderson I., Gelfand M.S., et al. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J. Bacteriol. 2003, 185:5673-5684.
16. Gidalevitz T., Prahlad V., Morimoto R.I. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb. Perspect. Biol. 2011, 3:3.
17. Gromiha M.M., Selvaraj S. Inter-residue interactions in protein folding and stability. Prog. Biophys. Mol. Biol. 2004, 86:235-277.
18. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
19. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009, 16:574-581.
20. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., Mann M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 2005, 4:1265-1272.
21. Janin J. Surface and inside volumes in globular proteins. Nature 1979, 277:491-492.
22. 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.
23. 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.
24. Lee H.C., Bernstein H.D. Trigger factor retards protein export in Escherichia coli. J. Biol. Chem. 2002, 277:43527-43535.
25. Maki J.A., Schnobrich D.J., Culver G.M. The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol. Cell 2002, 10:129-138.
26. Martinez-Hackert E., Hendrickson W.A. Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell 2009, 138:923-934.
27. Mayer M.P. Gymnastics of molecular chaperones. Mol. Cell 2010, 39:321-331.
28. McLennan N., Masters M. GroE is vital for cell-wall synthesis. Nature 1998, 392:139.
29. Nichols R.J., Sen S., Choo Y.J., Beltrao P., Zietek M., Chaba R., Lee S., Kazmierczak K.M., Lee K.J., Wong A., et al. Phenotypic landscape of a bacterial cell. Cell 2011, 144:143-156.
30. 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. USA 2009, 106:4201-4206.
31. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
32. Ong S.E., Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 2006, 1:2650-2660.
33. Raineri E., Ribeca P., Serrano L., Maier T. A more precise characterization of chaperonin substrates. Bioinformatics 2010, 26:1685-1689.
34. René O., Alix J.-H. Late steps of ribosome assembly in E. coli are sensitive to a severe heat stress but are assisted by the HSP70 chaperone machine. Nucleic Acids Res. 2011, 39:1855-1867.
35. Rüdiger S., Buchberger A., Bukau B. Interaction of Hsp70 chaperones with substrates. Nat. Struct. Biol. 1997, 4:342-349.
36. Schlecht R., Erbse A.H., Bukau B., Mayer M.P. Mechanics of Hsp70 chaperones enables differential interaction with client proteins. Nat. Struct. Mol. Biol. 2011, 18:345-351.
37. Smock R.G., Rivoire O., Russ W.P., Swain J.F., Leibler S., Ranganathan R., Gierasch L.M. An interdomain sector mediating allostery in Hsp70 molecular chaperones. Mol. Syst. Biol. 2010, 6:414.
38. Straus D., Walter W., Gross C.A. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 1990, 4(12A):2202-2209.
39. Tartaglia G.G., Dobson C.M., Hartl F.U., Vendruscolo M. Physicochemical determinants of chaperone requirements. J. Mol. Biol. 2010, 400:579-588.
40. Tartaglia G.G., Pawar A.P., Campioni S., Dobson C.M., Chiti F., Vendruscolo M. Prediction of aggregation-prone regions in structured proteins. J. Mol. Biol. 2008, 380:425-436.
41. Tartaglia G.G., Pechmann S., Dobson C.M., Vendruscolo M. Life on the edge: a link between gene expression levels and aggregation rates of human proteins. Trends Biochem. Sci. 2007, 32:204-206.
42. 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.
43. 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. USA 2007, 104:3101-3106.
44. Van Durme J., Maurer-Stroh S., Gallardo R., Wilkinson H., Rousseau F., Schymkowitz J. Accurate prediction of DnaK-peptide binding via homology modelling and experimental data. PLoS Comput. Biol. 2009, 5:e1000475.
45. Yu N.Y., Laird M.R., Spencer C., Brinkman F.S. PSORTdb-an expanded, auto-updated, user-friendly protein subcellular localization database for Bacteria and Archaea. Nucleic Acids Res. 2011, 39(Database issue):D241-D244.
46. 32 in vivo. J. Biol. Chem. 2005, 280:17758-17768.
47. Zhu X.T., Zhao X., Burkholder W.F., Gragerov A., Ogata C.M., Gottesman M.E., Hendrickson W.A. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996, 272:1606-1614.
48. Zhuravleva A., Gierasch L.M. Allosteric signal transmission in the nucleotide-binding domain of 70-kDa heat shock protein (Hsp70) molecular chaperones. Proc. Natl. Acad. Sci. USA 2011, 108:6987-6992.