Skip to main content

Substrate Interaction Networks of the Escherichia coli Chaperones: Trigger Factor, DnaK and GroEL

  • Chapter
Prokaryotic Systems Biology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 883))

Abstract

In the dense cellular environment, protein misfolding and inter-molecular protein aggregation compete with protein folding. Chaperones associate with proteins to prevent misfolding and to assist in folding to the native state. In Escherichia coli, the chaperones trigger factor, DnaK/DnaJ/GrpE, and GroEL/ES are the major chaperones responsible for insuring proper de novo protein folding. With multitudes of proteins produced by the bacterium, the chaperones have to be selective for their substrates. Yet, chaperone selectivity cannot be too specific. Recent biochemical and high-throughput studies have provided important insights highlighting the strategies used by chaperones in maintaining proteostasis in the cell. Here, we discuss the substrate networks and cooperation among these protein folding chaperones.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agashe VR, Guha S, Chang HC, 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

    Article  CAS  PubMed  Google Scholar 

  • Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230

    Article  CAS  PubMed  Google Scholar 

  • Baker TA, Sauer RT (2012) ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim Biophys Acta 1823:15–28

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barends TR, Werbeck ND, Reinstein J (2010) Disaggregases in 4 dimensions. Curr Opin Struct Biol 20:46–53

    Article  CAS  PubMed  Google Scholar 

  • Bertelsen EB, Chang L, Gestwicki JE, Zuiderweg ER (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci U~S~A 106:8471–8476

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL et al (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371:578–586

    Article  CAS  PubMed  Google Scholar 

  • Brehmer D, Rudiger S, Gassler CS, 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

    Article  CAS  PubMed  Google Scholar 

  • Brehmer D, Gassler C, Rist W, Mayer MP, Bukau B (2004) Influence of GrpE on DnaK-substrate interactions. J Biol Chem 279:27957–27964

    Article  CAS  PubMed  Google Scholar 

  • Buchberger A, Schroder H, Hesterkamp T, Schonfeld HJ, Bukau B (1996) Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J Mol Biol 261:328–333

    Article  CAS  PubMed  Google Scholar 

  • Bukau B, Walker GC (1989) Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol 171:2337–2346

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bukau B, Deuerling E, Pfund C, Craig EA (2000) Getting newly synthesized proteins into shape. Cell 101:119–122

    Article  CAS  PubMed  Google Scholar 

  • Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, Agostini F et al (2012) DnaK functions as a central hub in the E. coli chaperone network. Cell Rep 1:251–264

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekhar GN, Tilly K, Woolford C, Hendrix R, Georgopoulos C (1986) Purification and properties of the groES morphogenetic protein of Escherichia coli. J Biol Chem 261: 12414–12419

    CAS  PubMed  Google Scholar 

  • Chaudhry C, Farr GW, Todd MJ, Rye HS, Brunger AT, Adams PD et al (2003) Role of the gamma-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics. EMBO J 22:4877–4887

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheetham ME, Caplan AJ (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3:28–36

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen S, Roseman AM, Hunter AS, Wood SP, Burston SG, Ranson NA et al (1994) Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature 371:261–264

    Article  CAS  PubMed  Google Scholar 

  • Chenoweth MR, Trun N, Wickner S (2007) In vivo modulation of a DnaJ homolog, CbpA, by CbpM. J Bacteriol 189:3635–3638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chiti F, Calamai M, Taddei N, Stefani M, Ramponi G, Dobson CM (2002) Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc Natl Acad Sci U S A 99(Suppl 4):16419–16426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • DeLano WL (2002) The PyMOL molecular graphics system, Version 1.5.0.4 Schrödinger, LLC

    Google Scholar 

  • Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400:693–696

    Article  CAS  PubMed  Google Scholar 

  • Deuerling E, Patzelt H, Vorderwulbecke S, Rauch T, Kramer G, Schaffitzel E et al (2003) Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol Microbiol 47:1317–1328

    Article  CAS  PubMed  Google Scholar 

  • Dill KA, Chan HS (1997) From Levinthal to pathways to funnels. Nat Struct Biol 4:10–19

    Article  CAS  PubMed  Google Scholar 

  • Echave P, Esparza-Ceron MA, Cabiscol E, Tamarit J, Ros J, Membrillo-Hernandez J et al (2002) DnaK dependence of mutant ethanol oxidoreductases evolved for aerobic function and protective role of the chaperone against protein oxidative damage in Escherichia coli. Proc Natl Acad Sci U S A 99:4626–4631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ellis RJ (2006) Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31:395–401

    Article  CAS  PubMed  Google Scholar 

  • Ewalt KL, Hendrick JP, Houry WA, Hartl FU (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90:491–500

    Article  CAS  PubMed  Google Scholar 

  • Farr GW, Furtak K, Rowland MB, Ranson NA, Saibil HR, Kirchhausen T et al (2000) Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 100:561–573

    Article  CAS  PubMed  Google Scholar 

  • Fayet O, Ziegelhoffer T, Georgopoulos C (1989) The GroES and GroEL heat-shock gene-products of Escherichia-coli are essential for bacterial-growth at all temperatures. J Bacteriol 171: 1379–1385

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fenton WA, Kashi Y, Furtak K, Horwich AL (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371:614–619

    Article  CAS  PubMed  Google Scholar 

  • Ferbitz L, Maier T, Patzelt H, Bukau B, Deuerling E, Ban N (2004) Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431:590–596

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara K, Ishihama Y, Nakahigashi K, Soga T, Taguchi H (2010) A systematic survey of in vivo obligate chaperonin-dependent substrates. EMBO J 29:1552–1564

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fuzery AK, Tonelli M, Ta DT, Cornilescu G, Vickery LE, Markley JL (2008) Solution structure of the iron-sulfur cluster cochaperone HscB and its binding surface for the iron-sulfur assembly scaffold protein IscU. Biochemistry 47:9394–9404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gamer J, Multhaup G, Tomoyasu T, McCarty JS, Rudiger S, Schonfeld HJ 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Genest O, Hoskins JR, Camberg JL, Doyle SM, Wickner S (2011) Heat shock protein 90 from Escherichia coli collaborates with the DnaK chaperone system in client protein remodeling. Proc Natl Acad Sci U S A 108:8206–8211

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Genevaux P, Wawrzynow A, Zylicz M, Georgopoulos C, Kelley WL (2001) 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 276:7906–7912

    Article  CAS  PubMed  Google Scholar 

  • Genevaux P, Keppel F, Schwager F, Langendijk-Genevaux PS, Hartl FU, Georgopoulos C (2004) In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep 5:195–200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Genevaux P, Georgopoulos C, Kelley WL (2007) The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol Microbiol 66:840–857

    Article  CAS  PubMed  Google Scholar 

  • Georgescauld F, Popova K, Gupta AJ, Bracher A, Engen JR, Hayer-Hartl M et al (2014) GroEL/ES chaperonin modulates the mechanism and accelerates the rate of TIM-barrel domain folding. Cell 157:922–934

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD et al (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185:5673–5684

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goloubinoff P, Christeller JT, Gatenby AA, Lorimer GH (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP. Nature 342:884–889

    Article  CAS  PubMed  Google Scholar 

  • Grimshaw JP, Jelesarov I, Siegenthaler RK, Christen P (2003) Thermosensor action of GrpE. The DnaK chaperone system at heat shock temperatures. J Biol Chem 278:19048–19053

    Article  CAS  PubMed  Google Scholar 

  • Gur E, Biran D, Shechter N, Genevaux P, Georgopoulos C, Ron EZ (2004) The Escherichia coli DjlA and CbpA proteins can substitute for DnaJ in DnaK-mediated protein disaggregation. J Bacteriol 186:7236–7242

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gur E, Katz C, Ron EZ (2005) All three J-domain proteins of the Escherichia coli DnaK chaperone machinery are DNA binding proteins. FEBS Lett 579:1935–1939

    Article  CAS  PubMed  Google Scholar 

  • Harrison C (2003) GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8: 218–224

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F, 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

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    Article  CAS  PubMed  Google Scholar 

  • Hennessy F, Nicoll WS, Zimmermann R, Cheetham ME, Blatch GL (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci 14:1697–1709

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hesterkamp T, Hauser S, Lutcke H, Bukau B (1996) Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains. Proc Natl Acad Sci U S A 93: 4437–4441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoffmann JH, Linke K, Graf PC, Lilie H, Jakob U (2004) Identification of a redox-regulated chaperone network. EMBO J 23:160–168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoffmann A, Merz F, Rutkowska A, Zachmann-Brand B, Deuerling E, Bukau B (2006) Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J Biol Chem 281:6539–6545

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann A, Bukau B, Kramer G (2010) Structure and function of the molecular chaperone trigger factor. Biochim Biophys Acta 1803:650–661

    Article  CAS  PubMed  Google Scholar 

  • Horwich AL, Low KB, Fenton WA, Hirshfield IN, Furtak K (1993) Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 74:909–917

    Article  CAS  PubMed  Google Scholar 

  • Horwich AL, Farr GW, Fenton WA (2006) GroEL-GroES-mediated protein folding. Chem Rev 106:1917–1930

    Article  CAS  PubMed  Google Scholar 

  • Houry WA, Frishman D, Eckerskorn C, Lottspeich F, Hartl FU (1999) Identification of in vivo substrates of the chaperonin GroEL. Nature 402:147–154

    Article  CAS  PubMed  Google Scholar 

  • Huang K, Flanagan JM, Prestegard JH (1999) The influence of C-terminal extension on the structure of the “J-domain” in E. coli DnaJ. Protein Sci 8:203–214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hunt JF, Weaver AJ, Landry SJ, Gierasch L, Deisenhofer J (1996) The crystal structure of the GroES co-chaperonin at 2.8 A resolution. Nature 379:37–45

    Article  CAS  PubMed  Google Scholar 

  • Kaiser CM, Chang HC, Agashe VR, Lakshmipathy SK, Etchells SA, Hayer-Hartl M et al (2006) Real-time observation of trigger factor function on translating ribosomes. Nature 444:455–460

    Article  CAS  PubMed  Google Scholar 

  • Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karzai AW, McMacken R (1996) A bipartite signaling mechanism involved in DnaJ-mediated activation of the Escherichia coli DnaK protein. J Biol Chem 271:11236–11246

    Article  CAS  PubMed  Google Scholar 

  • Kelley WL (1998) The J-domain family and the recruitment of chaperone power. Trends Biochem Sci 23:222–227

    Article  CAS  PubMed  Google Scholar 

  • Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang HC, Stines AP et al (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122:209–220

    Article  CAS  PubMed  Google Scholar 

  • Kityk R, Kopp J, Sinning I, Mayer MP (2012) Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol Cell 48:863–874

    Article  CAS  PubMed  Google Scholar 

  • Kluck CJ, Patzelt H, Genevaux P, Brehmer D, Rist W, Schneider-Mergener J et al (2002) Structure-function analysis of HscC, the Escherichia coli member of a novel subfamily of specialized Hsp70 chaperones. J Biol Chem 277:41060–41069

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Sourjik V (2012) Physical map and dynamics of the chaperone network in Escherichia coli. Mol Microbiol 84:736–747

    Article  CAS  PubMed  Google Scholar 

  • Lakshmipathy SK, Tomic S, Kaiser CM, Chang HC, Genevaux P, Georgopoulos C et al (2007) Identification of nascent chain interaction sites on trigger factor. J Biol Chem 282:12186–12193

    Article  CAS  PubMed  Google Scholar 

  • Langer T, Pfeifer G, Martin J, Baumeister W, Hartl FU (1992) Chaperonin-mediated protein folding – GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J 11:4757–4765

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laskowska E, Wawrzynow A, Taylor A (1996) IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–122

    Article  CAS  PubMed  Google Scholar 

  • Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, Reinstein J et al (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci U S A 96: 5452–5457

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liberek K, Marszalek J, Ang D, Georgopoulos C, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lill R, Crooke E, Guthrie B, Wickner W (1988) The “trigger factor cycle” includes ribosomes, presecretory proteins, and the plasma membrane. Cell 54:1013–1018

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Puchalla J, Shoup D, Rye HS (2013) Repetitive protein unfolding by the trans ring of the GroEL-GroES chaperonin complex stimulates folding. J Biol Chem 288:30944–30955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maier R, Eckert B, Scholz C, Lilie H, Schmid FX (2003) Interaction of trigger factor with the ribosome. J Mol Biol 326:585–592

    Article  CAS  PubMed  Google Scholar 

  • Mally A, Witt SN (2001) GrpE accelerates peptide binding and release from the high affinity state of DnaK. Nat Struct Biol 8:254–257

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Hackert E, Hendrickson WA (2009) Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell 138:923–934

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martinez-Yamout M, Legge GB, Zhang O, Wright PE, Dyson HJ (2000) Solution structure of the cysteine-rich domain of the Escherichia coli chaperone protein DnaJ. J Mol Biol 300:805–818

    Article  CAS  PubMed  Google Scholar 

  • Mashaghi A, Kramer G, Bechtluft P, Zachmann-Brand B, Driessen AJ, Bukau B et al (2013) Reshaping of the conformational search of a protein by the chaperone trigger factor. Nature 500:98–101

    Article  CAS  PubMed  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mayor U, Guydosh NR, Johnson CM, Grossmann JG, Sato S, Jas GS et al (2003) The complete folding pathway of a protein from nanoseconds to microseconds. Nature 421:863–867

    Article  CAS  PubMed  Google Scholar 

  • Merz F, Hoffmann A, Rutkowska A, Zachmann-Brand B, Bukau B, Deuerling E (2006) The C-terminal domain of Escherichia coli trigger factor represents the central module of its chaperone activity. J Biol Chem 281:31963–31971

    Article  CAS  PubMed  Google Scholar 

  • Miot M, Reidy M, Doyle SM, Hoskins JR, Johnston DM, Genest O et al (2011) Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc Natl Acad Sci U S A 108:6915–6920

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mogk A, Tomoyasu T, Goloubinoff P, Rudiger S, Roder D, Langen H et al (1999) Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J 18:6934–6949

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R et al (2011) Phenotypic landscape of a bacterial cell. Cell 144:143–156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niwa T, Kanamori T, Ueda T, Taguchi H (2012) Global analysis of chaperone effects using a reconstituted cell-free translation system. Proc Natl Acad Sci U S A 109:8937–8942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oh E, Becker AH, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Packschies L, Theyssen H, Buchberger A, Bukau B, Goody RS, Reinstein J (1997) GrpE accelerates nucleotide exchange of the molecular chaperone DnaK with an associative displacement mechanism. Biochemistry 36:3417–3422

    Article  CAS  PubMed  Google Scholar 

  • Patzelt H, Rudiger S, Brehmer D, Kramer G, Vorderwulbecke S, Schaffitzel E et al (2001) Binding specificity of Escherichia coli trigger factor. Proc Natl Acad Sci U S A 98:14244–14249

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raine A, Lovmar M, Wikberg J, Ehrenberg M (2006) Trigger factor binding to ribosomes with nascent peptide chains of varying lengths and sequences. J Biol Chem 281:28033–28038

    Article  CAS  PubMed  Google Scholar 

  • Randall LL, Hardy SJ (2002) SecB, one small chaperone in the complex milieu of the cell. Cell Mol Life Sci 59:1617–1623

    Article  CAS  PubMed  Google Scholar 

  • Ranson NA, Farr GW, Roseman AM, Gowen B, Fenton WA, Horwich AL et al (2001) ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107:869–879

    Article  CAS  PubMed  Google Scholar 

  • Ranson NA, Clare DK, Farr GW, Houldershaw D, Horwich AL, Saibil HR (2006) Allosteric signaling of ATP hydrolysis in GroEL-GroES complexes. Nat Struct Mol Biol 13:147–152

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rosenzweig R, Moradi S, Zarrine-Afsar A, Glover JR, Kay LE (2013) Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction. Science 339:1080–1083

    Article  CAS  PubMed  Google Scholar 

  • Rudiger S, Germeroth L, Schneider-Mergener J, Bukau B (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16:1501–1507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rudiger S, Schneider-Mergener J, Bukau B (2001) Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. EMBO J 20:1042–1050

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rutkowska A, Mayer MP, Hoffmann A, Merz F, Zachmann-Brand B, Schaffitzel C et al (2008) Dynamics of trigger factor interaction with translating ribosomes. J Biol Chem 283:4124–4132

    Article  CAS  PubMed  Google Scholar 

  • Rye HS, Roseman AM, Chen S, Furtak K, Fenton WA, Saibil HR et al (1999) GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 97: 325–338

    Article  CAS  PubMed  Google Scholar 

  • Saibil HR, Fenton WA, Clare DK, Horwich AL (2013) Structure and allostery of the chaperonin GroEL. J Mol Biol 425:1476–1487

    Article  CAS  PubMed  Google Scholar 

  • Saio T, Guan X, Rossi P, Economou A, Kalodimos CG (2014) Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science 344:1250494

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schlecht R, Erbse AH, Bukau B, Mayer MP (2011) Mechanics of Hsp70 chaperones enables differential interaction with client proteins. Nat Struct Mol Biol 18:345–351

    Article  CAS  PubMed  Google Scholar 

  • Schonfeld HJ, Schmidt D, Schroder H, Bukau B (1995) The DnaK chaperone system of Escherichia coli: quaternary structures and interactions of the DnaK and GrpE components. J Biol Chem 270:2183–2189

    Article  CAS  PubMed  Google Scholar 

  • Sell SM, Eisen C, Ang D, Zylicz M, Georgopoulos C (1990) Isolation and characterization of dnaJ null mutants of Escherichia coli. J Bacteriol 172:4827–4835

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shi W, Zhou Y, Wild J, Adler J, Gross CA (1992) DnaK, DnaJ, and GrpE are required for flagellum synthesis in Escherichia coli. J Bacteriol 174:6256–6263

    PubMed Central  CAS  PubMed  Google Scholar 

  • Silberg JJ, Hoff KG, Vickery LE (1998) The Hsc66-Hsc20 chaperone system in Escherichia coli: chaperone activity and interactions with the DnaK-DnaJ-grpE system. J Bacteriol 180: 6617–6624

    PubMed Central  CAS  PubMed  Google Scholar 

  • Srinivasan SR, Gillies AT, Chang L, Thompson AD, Gestwicki JE (2012) Molecular chaperones DnaK and DnaJ share predicted binding sites on most proteins in the E. coli proteome. Mol Biosyst 8:2323–2333

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Szabo A, Langer T, Schroder H, Flanagan J, Bukau B, Hartl FU (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc Natl Acad Sci U S A 91:10345–10349

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tartaglia GG, Pechmann S, Dobson CM, Vendruscolo M (2007) Life on the edge: a link between gene expression levels and aggregation rates of human proteins. Trends Biochem Sci 32: 204–206

    Article  CAS  PubMed  Google Scholar 

  • Tartaglia GG, Dobson CM, Hartl FU, Vendruscolo M (2010) Physicochemical determinants of chaperone requirements. J Mol Biol 400:579–588

    Article  CAS  PubMed  Google Scholar 

  • Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Teter SA, Houry WA, 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

    Article  CAS  PubMed  Google Scholar 

  • Ueguchi C, Kakeda M, Yamada H, Mizuno T (1994) An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc Natl Acad Sci U S A 91:1054–1058

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ullers RS, Luirink J, Harms N, Schwager F, Georgopoulos C, Genevaux P (2004) SecB is a bona fide generalized chaperone in Escherichia coli. Proc Natl Acad Sci U S A 101:7583–7588

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ung PM, Thompson AD, Chang L, Gestwicki JE, Carlson HA (2013) Identification of key hinge residues important for nucleotide-dependent allostery in E. coli Hsp70/DnaK. PLoS Comput Biol 9:e1003279

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vabulas RM, Raychaudhuri S, Hayer-Hartl M, Hartl FU (2010) Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb Perspect Biol 2:a004390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Valent QA, Kendall DA, High S, Kusters R, Oudega B, 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wall D, Zylicz M, Georgopoulos C (1994) The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication. J Biol Chem 269:5446–5451

    CAS  PubMed  Google Scholar 

  • Weaver J, Rye HS (2014) The C-terminal tails of the bacterial chaperonin GroEL stimulate protein folding by directly altering the conformation of a substrate protein. J Biol Chem 289: 23219–23232

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wild J, Altman E, Yura T, Gross CA (1992) DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev 6:1165–1172

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388:741–750

    Article  CAS  PubMed  Google Scholar 

  • Yifrach O, Horovitz A (1995) Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34:5303–5308

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME et al (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606–1614

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Vaibhav Bhandari was the recipient of a Jaro Sodek Award—Ontario Student Opportunity Trust Fund (OSOTF) fellowship from the Department of Biochemistry at the University of Toronto. This work was supported by a grant from the Canadian Institutes of Health Research (MOP-130374) to WAH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Walid A. Houry .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Bhandari, V., Houry, W.A. (2015). Substrate Interaction Networks of the Escherichia coli Chaperones: Trigger Factor, DnaK and GroEL. In: Krogan, PhD, N., Babu, PhD, M. (eds) Prokaryotic Systems Biology. Advances in Experimental Medicine and Biology, vol 883. Springer, Cham. https://doi.org/10.1007/978-3-319-23603-2_15

Download citation

Publish with us

Policies and ethics