Skip to main content
SpringerLink
Log in

Systems-Level Analysis of Protein Quality in Inclusion Body-Forming Escherichia coli Cells

  • Chapter
Systems Biology and Biotechnology of Escherichia coli

Abstract

Recombinant proteins produced in Escherichia coli often aggregate as amorphous masses of insoluble material known as inclusion bodies. Being quite homogeneous in their composition, inclusion bodies display amyloid-like properties such as sequence-dependent protein-protein interactions, seeding-driven deposition of their components and β-sheet intermolecular architecture. However, inclusion bodies formed by different proteins and enzymes also show important extents of native-like secondary structure and include significant proportions of properly folded, functional protein, which makes them suitable to be used in catalytic processes. Inclusion bodies are formed as a result of the incapability of the quality control cell system to cope with the non physiological amounts of misfolding-prone proteins produced upon recombinant gene expression. Multiple cellular proteins involved in the quality control, namely chaperones and proteases, participate in their formation and co-ordinately determine the amount of aggregated protein, the size of aggregates and the main structural and functional properties of the embedded polypeptides, such as their inner molecular organization.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Allen SP, Polazzi JO, Gierse JK et al. (1992) Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol 174(21):6938–47

    PubMed  CAS  Google Scholar 

  • Ami D, Bonecchi L, Cali S et al. (2003) FT-IR study of heterologous protein expression in recombinant Escherichia coli strains. Biochim Biophys Acta 1624(1–3):6–10

    Google Scholar 

  • Ami D, Natalello A, Gatti-Lafranconi P et al. (2005) Kinetics of inclusion body formation studied in intact cells by FT-IR spectroscopy. FEBS Lett 579(16):3433–6

    PubMed  CAS  Google Scholar 

  • Ami D, Natalello A, Taylor G et al. (2006) Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim Biophys Acta 1764(4):793–9

    PubMed  CAS  Google Scholar 

  • Amrein KE, Takacs B, Stieger M et al. (1995) Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc Natl Acad Sci USA 92(4):1048–52

    PubMed  CAS  Google Scholar 

  • Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181(96):223–30

    PubMed  CAS  Google Scholar 

  • Apiyo D, Wittung-Stafshede P (2002) Presence of the cofactor speeds up folding of Desulfovibrio desulfuricans flavodoxin. Protein Sci 11(5):1129–35

    PubMed  CAS  Google Scholar 

  • Baldwin RL (1986) Temperature dependence of the hydrophobic interaction in protein folding. Proc Natl Acad Sci USA 83(21):8069–72

    PubMed  CAS  Google Scholar 

  • Baldwin RL (1994) Protein folding. Matching speed and stability. Nature 369(6477):183–4

    CAS  Google Scholar 

  • Baneyx F (2004) Keeping up with protein folding. Microb Cell Fact 3(1):6

    PubMed  Google Scholar 

  • Baneyx F, Georgiou G (1991) Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecular-weight substrates in vivo. J Bacteriol 173(8):2696–703

    PubMed  CAS  Google Scholar 

  • Ben-Zvi AP, Goloubinoff P (2001) Review: mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 135(2):84–93

    PubMed  CAS  Google Scholar 

  • Bowden GA, Paredes AM, Georgiou G (1991) Structure and morphology of protein inclusion bodies in Escherichia coli. Biotechnology (N Y) 9(8):725–30

    CAS  Google Scholar 

  • Bruser T, Yano T, Brune DC et al. (2003) Membrane targeting of a folded and cofactor-containing protein. Eur J Biochem 270(6):1211–21

    PubMed  CAS  Google Scholar 

  • Bucciantini M, Calloni G, Chiti F et al. (2004) Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J Biol Chem 279(30):31374–82

    PubMed  CAS  Google Scholar 

  • Bucciantini M, Giannoni E, Chiti F et al. (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416(6880):507–11

    PubMed  CAS  Google Scholar 

  • Bukau B (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9(4): 671–80

    PubMed  CAS  Google Scholar 

  • Bukau B, Deuerling E, Pfund C et al. (2000) Getting newly synthesized proteins into shape. Cell 101(2):119–22

    PubMed  CAS  Google Scholar 

  • Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125(3):443–51

    PubMed  CAS  Google Scholar 

  • Carbonell X, Villaverde A (2002) Protein aggregated into bacterial inclusion bodies does not result in protection from proteolytic digestion. Biotechnol Lett 24(23):1939–1944

    CAS  Google Scholar 

  • Carrio M, Gonzalez-Montalban N, Vera A et al. (2005) Amyloid-like properties of bacterial inclusion bodies. J Mol Biol 347(5):1025–37

    PubMed  CAS  Google Scholar 

  • Carrio MM, Corchero JL, Villaverde A (1998) Dynamics of in vivo protein aggregation: building inclusion bodies in recombinant bacteria. FEMS Microbiol Lett 169(1):9–15

    PubMed  CAS  Google Scholar 

  • Carrio MM, Corchero JL, Villaverde A (1999) Proteolytic digestion of bacterial inclusion body proteins during dynamic transition between soluble and insoluble forms. Biochim Biophys Acta 1434(1):170–6

    PubMed  CAS  Google Scholar 

  • Carrio MM, Villaverde A (2001) Protein aggregation as bacterial inclusion bodies is reversible. FEBS Lett 489(1):29–33

    PubMed  CAS  Google Scholar 

  • Carrio MM, Villaverde A (2002) Construction and deconstruction of bacterial inclusion bodies. J Biotechnol 96(1):3–12

    PubMed  CAS  Google Scholar 

  • Carrio MM, Villaverde A (2003) Role of molecular chaperones in inclusion body formation. FEBS Lett 537(1–3):215–21

    PubMed  CAS  Google Scholar 

  • Carrio MM, Villaverde A (2005) Localization of chaperones DnaK and GroEL in bacterial inclusion bodies. J Bacteriol 187(10):3599–601

    PubMed  CAS  Google Scholar 

  • Chapman D, Haris PI (1989) Biomembrane structures. Fourier transform infrared spectroscopy and biomembrane technology. Biochem Soc Trans 17(6):951–3

    CAS  Google Scholar 

  • Chapman E, Farr GW, Usaite R et al. (2006) Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL. Proc Natl Acad Sci USA 103(43):15800–5

    PubMed  CAS  Google Scholar 

  • Chesshyre JA, Hipkiss AR (1989) Low temperatures stabilize interferon α-2 against proteolysis in Methylophilus methylotrophus and Escherichia coli. Appl Microbiol Biotechnol 31(2): 158–162

    CAS  Google Scholar 

  • Chiti F, Taddei N, van Nuland NA et al. (1998) Structural characterization of the transition state for folding of muscle acylphosphatase. J Mol Biol 283(4):893–903

    PubMed  CAS  Google Scholar 

  • Chuang SE, Burland V, Plunkett G, 3rd et al. (1993) Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene 134(1):1–6

    PubMed  CAS  Google Scholar 

  • Clark ED (2001) Protein refolding for industrial processes. Curr Opin Biotechnol 12(2):202–7

    PubMed  CAS  Google Scholar 

  • Corchero JL, Cubarsi R, Enfors S et al. (1997) Limited in vivo proteolysis of aggregated proteins. Biochem Biophys Res Commun 237(2):325–30

    PubMed  CAS  Google Scholar 

  • Cubarsi R, Carrio MM, Villaverde A (2005) A mathematical approach to molecular organization and proteolytic disintegration of bacterial inclusion bodies. Math Med Biol 22(3):209–26

    PubMed  CAS  Google Scholar 

  • Dale GE, Schonfeld HJ, Langen H et al. (1994) Increased solubility of trimethoprim-resistant type S1 DHFR from Staphylococcus aureus in Escherichia coli cells overproducing the chaperonins GroEL and GroES. Protein Eng 7(7):925–31

    PubMed  CAS  Google Scholar 

  • de Groot NS, Ventura S (2006) Protein activity in bacterial inclusion bodies correlates with predicted aggregation rates. J Biotechnol 125(1):110–3

    PubMed  Google Scholar 

  • de Marco A, Deuerling E, Mogk A et al. (2007) Chaperone-based procedure to increase yields of soluble recombinant proteins produced in E. coli. BMC Biotechnol 7:32

    PubMed  Google Scholar 

  • de Marco A, Volrath S, Bruyere T et al. (2000) Recombinant maize protoporphyrinogen IX oxidase expressed in Escherichia coli forms complexes with GroEL and DnaK chaperones. Protein Expr Purif 20(1):81–6

    PubMed  Google Scholar 

  • Dill KA, Chan HS (1997) From Levinthal to pathways to funnels. Nat Struct Biol 4(1):10–9

    PubMed  CAS  Google Scholar 

  • Dinner AR, Sali A, Smith LJ et al. (2000) Understanding protein folding via free-energy surfaces from theory and experiment. Trends Biochem Sci 25(7):331–9

    PubMed  CAS  Google Scholar 

  • Dobson CM (2004) Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 15(1):3–16

    PubMed  CAS  Google Scholar 

  • Echave P, Esparza-Ceron MA, Cabiscol E 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 USA 99(7):4626–31

    PubMed  CAS  Google Scholar 

  • Ehrnsperger M, Graber S, Gaestel M et al. (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. Embo J 16(2):221–9

    PubMed  CAS  Google Scholar 

  • Ellis J (1987) Proteins as molecular chaperones. Nature 328(6129):378–9

    PubMed  CAS  Google Scholar 

  • Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26(10):597–604

    PubMed  CAS  Google Scholar 

  • Enfors SO (1992) Control of in vivo proteolysis in the production of recombinant proteins. Trends Biotechnol 10(9):310–5

    PubMed  CAS  Google Scholar 

  • Esposito D, Chatterjee DK (2006) Enhancement of soluble protein expression through the use of fusion tags. Curr Opin Biotechnol 17(4):353–8

    PubMed  CAS  Google Scholar 

  • Estapè D, Rinas U (1996) Optimized procedures for purification and solubilization of basic fibroblast growth factor inclusion bodies. Biotechnol. Tech 10(7):481–484

    Google Scholar 

  • Ewalt KL, Hendrick JP, Houry WA et al. (1997) In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90(3):491–500

    PubMed  CAS  Google Scholar 

  • Fahnert B, Lilie H, Neubauer P (2004) Inclusion bodies: formation and utilisation. Adv Biochem Eng Biotechnol 89:93–142

    PubMed  CAS  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(3): 1379–85

    PubMed  CAS  Google Scholar 

  • Ferrer M, Chernikova TN, Yakimov MM et al. (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21(11):1266–7

    PubMed  CAS  Google Scholar 

  • Fink AL (1998) Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des 3(1):R9–23

    PubMed  CAS  Google Scholar 

  • Fredriksson A, Ballesteros M, Dukan S et al. (2005) Defense against protein carbonylation by DnaK/DnaJ and proteases of the heat shock regulon. J Bacteriol 187(12):4207–13

    PubMed  CAS  Google Scholar 

  • Garcia-Fruitos E, Aris A, Villaverde A (2007a) Localization of functional polypeptides in bacterial inclusion bodies. Appl Environ Microbiol 73(1):289–94

    PubMed  CAS  Google Scholar 

  • Garcia-Fruitos E, Carrio MM, Aris A et al. (2005a) Folding of a misfolding-prone beta-galactosidase in absence of DnaK. Biotechnol Bioeng 90(7):869–75

    PubMed  CAS  Google Scholar 

  • Garcia-Fruitos E, Gonzalez-Montalban N, Morell M et al. (2005b) Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb Cell Fact 4:27

    PubMed  Google Scholar 

  • Garcia-Fruitos E, Martinez-Alonso M, Gonzalez-Montalban N et al. (2007b) Divergent genetic control of protein solubility and conformational quality in Escherichia coli. J Mol Biol 374(1):195–205

    PubMed  CAS  Google Scholar 

  • Gasser B, Saloheimo M, Rinas U et al. (2008) Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb Cell Fact 7:11

    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(4):840–57

    PubMed  CAS  Google Scholar 

  • Genevaux P, Schwager F, Georgopoulos C et al. (2001) The djlA gene acts synergistically with dnaJ in promoting Escherichia coli growth. J Bacteriol 183(19):5747–50

    PubMed  CAS  Google Scholar 

  • Georgiou G, Valax P (1996) Expression of correctly folded proteins in Escherichia coli. Curr Opin Biotechnol 7(2):190–7

    PubMed  CAS  Google Scholar 

  • Georgiou G, Valax P, Ostermeier M et al. (1994) Folding and aggregation of TEM beta-lactamase: analogies with the formation of inclusion bodies in Escherichia coli. Protein Sci 3(11):1953–60

    PubMed  CAS  Google Scholar 

  • Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355(6355):33–45

    PubMed  CAS  Google Scholar 

  • Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94(1):73–82

    PubMed  CAS  Google Scholar 

  • Glover JR, Tkach JM (2001) Crowbars and ratchets: hsp100 chaperones as tools in reversing protein aggregation. Biochem Cell Biol 79(5):557–68

    PubMed  CAS  Google Scholar 

  • Goloubinoff P, Mogk A, Zvi AP et al. (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA 96(24): 13732–7

    PubMed  CAS  Google Scholar 

  • Gonzalez-Montalban N, Garcia-Fruitos E, Ventura S et al. (2006) The chaperone DnaK controls the fractioning of functional protein between soluble and insoluble cell fractions in inclusion body-forming cells. Microb Cell Fact 5:26

    PubMed  Google Scholar 

  • Gonzalez-Montalban N, Garcia-Fruitos E, Villaverde A (2007a) Recombinant protein solubility – does more mean better? Nat Biotechnol 25(7):718–20

    Google Scholar 

  • Gonzalez-Montalban N, Natalello A, Garcia-Fruitos E et al. (2008) In situ protein folding and activation in bacterial inclusion bodies. Biotechnol Bioeng 100(4):797–802

    PubMed  CAS  Google Scholar 

  • Gonzalez-Montalban N, Villaverde A, Aris A (2007b) Amyloid-linked cellular toxicity triggered by bacterial inclusion bodies. Biochem Biophys Res Commun 355(3):637–42

    PubMed  CAS  Google Scholar 

  • Gottesman S, Wickner S, Maurizi MR (1997) Protein quality control: triage by chaperones and proteases. Genes Dev 11(7):815–23

    PubMed  CAS  Google Scholar 

  • Graf PC, Jakob U (2002) Redox-regulated molecular chaperones. Cell Mol Life Sci 59(10): 1624–31

    PubMed  CAS  Google Scholar 

  • Grantcharova V, Alm EJ, Baker D et al. (2001) Mechanisms of protein folding. Curr Opin Struct Biol 11(1):70–82

    PubMed  CAS  Google Scholar 

  • Grudzielanek S, Velkova A, Shukla A et al. (2007) Cytotoxicity of insulin within its self-assembly and amyloidogenic pathways. J Mol Biol 370(2):372–84

    PubMed  CAS  Google Scholar 

  • Gupta RS, Singh B (1994) Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus. Curr Biol 4(12):1104–14

    PubMed  CAS  Google Scholar 

  • Han MJ, Park SJ, Park TJ et al. (2004) Roles and applications of small heat shock proteins in the production of recombinant proteins in Escherichia coli. Biotechnol Bioeng 88(4): 426–36

    PubMed  CAS  Google Scholar 

  • Harris TJ, Patel T, Marston FA et al. (1986) Cloning of cDNA coding for human tissue-type plasminogen activator and its expression in Escherichia coli. Mol Biol Med 3(3):279–92

    PubMed  CAS  Google Scholar 

  • Hart RA, Rinas U, Bailey JE (1990) Protein composition of Vitreoscilla hemoglobin inclusion bodies produced in Escherichia coli. J Biol Chem 265(21):12728–33

    PubMed  CAS  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295(5561):1852–8

    PubMed  CAS  Google Scholar 

  • Hartley DL, Kane JF (1988) Properties of inclusion bodies from recombinant Escherichia coli. Biochem Soc Trans 16(2):101–2

    PubMed  CAS  Google Scholar 

  • Haslbeck M (2002) sHsps and their role in the chaperone network. Cell Mol Life Sci 59(10): 1649–57

    PubMed  CAS  Google Scholar 

  • Hennessy F, Nicoll WS, Zimmermann R et al. (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci 14(7):1697–709

    PubMed  CAS  Google Scholar 

  • Hoffmann F, Rinas U (2000) Kinetics of heat-shock response and inclusion body formation during temperature-induced production of basic fibroblast growth factor in high-cell-density cultures of recombinant Escherichia coli. Biotechnol Prog 16(6):1000–7

    PubMed  CAS  Google Scholar 

  • Hoffmann F, Rinas U (2001) On-line estimation of the metabolic burden resulting from the synthesis of plasmid-encoded and heat-shock proteins by monitoring respiratory energy generation. Biotechnol Bioeng 76(4):333–40

    PubMed  CAS  Google Scholar 

  • Hoffmann F, Rinas U (2004) Roles of heat-shock chaperones in the production of recombinant proteins in Escherichia coli. Adv Biochem Eng Biotechnol 89:143–61

    PubMed  CAS  Google Scholar 

  • Hoskins JR, Pak M, Maurizi MR et al. (1998) The role of the ClpA chaperone in proteolysis by ClpAP. Proc Natl Acad Sci USA 95(21):12135–40

    PubMed  CAS  Google Scholar 

  • Huang GC, Li ZY, Zhou JM et al. (2000) Assisted folding of D-glyceraldehyde-3-phosphate dehydrogenase by trigger factor. Protein Sci 9(6):1254–61

    PubMed  CAS  Google Scholar 

  • Hunke S, Betton JM (2003) Temperature effect on inclusion body formation and stress response in the periplasm of Escherichia coli. Mol Microbiol 50(5):1579–89

    PubMed  CAS  Google Scholar 

  • Hunt C, Morimoto RI (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci USA 82(19): 6455–9

    PubMed  CAS  Google Scholar 

  • Ivanova MI, Sawaya MR, Gingery M et al. (2004) An amyloid-forming segment of beta2-microglobulin suggests a molecular model for the fibril. Proc Natl Acad Sci USA 101(29):10584–9

    PubMed  CAS  Google Scholar 

  • Jackson SE (1998) How do small single-domain proteins fold? Fold Des 3(4):R81–91

    PubMed  CAS  Google Scholar 

  • Jevsevar S, Gaberc-Porekar V, Fonda I et al. (2005) Production of nonclassical inclusion bodies from which correctly folded protein can be extracted. Biotechnol Prog 21(2):632–9

    PubMed  CAS  Google Scholar 

  • Jungbauer A, Kaar W (2007) Current status of technical protein refolding. J Biotechnol 128(3):587–96

    PubMed  CAS  Google Scholar 

  • Jurgen B, Lin HY, Riemschneider S et al. (2000) Monitoring of genes that respond to overproduction of an insoluble recombinant protein in Escherichia coli glucose-limited fed-batch fermentations. Biotechnol Bioeng 70(2):217–24

    PubMed  CAS  Google Scholar 

  • Kapust RB, Tozser J, Copeland TD et al. (2002) The P1′ specificity of tobacco etch virus protease. Biochem Biophys Res Commun 294(5):949–55

    PubMed  CAS  Google Scholar 

  • Kapust RB, Tozser J, Fox JD et al. (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng 14(12): 993–1000

    PubMed  CAS  Google Scholar 

  • Karplus M (1997) The Levinthal paradox: yesterday and today. Fold Des 2(4):S69–75

    PubMed  CAS  Google Scholar 

  • Kazemi-Esfarjani P, Benzer S (2000) Genetic suppression of polyglutamine toxicity in Drosophila. Science 287(5459):1837–40

    PubMed  CAS  Google Scholar 

  • Kedzierska S, Staniszewska M, Wegrzyn A et al. (1999) The role of DnaK/DnaJ and GroEL/GroES systems in the removal of endogenous proteins aggregated by heat-shock from Escherichia coli cells. FEBS Lett 446(2–3):331–7

    PubMed  CAS  Google Scholar 

  • Kerner MJ, Naylor DJ, Ishihama Y et al. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122(2):209–20

    PubMed  CAS  Google Scholar 

  • Khan F, Chuang JI, Gianni S et al. (2003) The kinetic pathway of folding of barnase. J Mol Biol 333(1):169–86

    PubMed  CAS  Google Scholar 

  • Kitagawa M, Miyakawa M, Matsumura Y et al. (2002) Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269(12):2907–17

    PubMed  CAS  Google Scholar 

  • Krobitsch S, Lindquist S (2000) Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc Natl Acad Sci USA 97(4):1589–94

    PubMed  CAS  Google Scholar 

  • Kuczynska-Wisnik D, Kedzierska S, Matuszewska E et al. (2002) The Escherichia coli small heat-shock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock. Microbiology 148(Pt 6):1757–65

    PubMed  CAS  Google Scholar 

  • Kuczynska-Wisnik D, Zurawa-Janicka D, Narkiewicz J et al. (2004) Escherichia coli small heat shock proteins IbpA/B enhance activity of enzymes sequestered in inclusion bodies. Acta Biochim Pol 51(4):925–31

    PubMed  CAS  Google Scholar 

  • Laskey RA, Honda BM, Mills AD et al. (1978) Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275(5679):416–20

    PubMed  CAS  Google Scholar 

  • Laskowska E, Bohdanowicz J, Kuczynska-Wisnik D et al. (2004) Aggregation of heat-shock-denatured, endogenous proteins and distribution of the IbpA/B and Fda marker-proteins in Escherichia coli WT and grpE280 cells. Microbiology 150(Pt 1):247–59

    PubMed  CAS  Google Scholar 

  • Lemaux PG, Herendeen SL, Bloch PL et al. (1978) Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell 13(3):427–34

    PubMed  CAS  Google Scholar 

  • Lethanh H, Neubauer P, Hoffmann F (2005) The small heat-shock proteins IbpA and IbpB reduce the stress load of recombinant Escherichia coli and delay degradation of inclusion bodies. Microb Cell Fact 4(1):6

    PubMed  Google Scholar 

  • Levchenko I, Luo L, Baker TA (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9(19):2399–408

    PubMed  CAS  Google Scholar 

  • Lewandowska A, Matuszewska M, Liberek K (2007) Conformational properties of aggregated polypeptides determine ClpB-dependence in the disaggregation process. J Mol Biol 371(3):800–11

    PubMed  CAS  Google Scholar 

  • Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–77

    PubMed  CAS  Google Scholar 

  • Malki A, Kern R, Abdallah J et al. (2003) Characterization of the Escherichia coli YedU protein as a molecular chaperone. Biochem Biophys Res Commun 301(2):430–6

    PubMed  CAS  Google Scholar 

  • Marston FA (1986) The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem J 240(1):1–12

    PubMed  CAS  Google Scholar 

  • Marston FA, Hartley DL (1990) Solubilization of protein aggregates. Methods Enzymol 182: 264–76

    PubMed  CAS  Google Scholar 

  • Marston FAO, Lowe PA, Doel MT et al. (1984) Purification of Calf Prochymosin(Prorennin) Synthesized in Escherichia coli. Bio/Technology 2(9):800–804

    CAS  Google Scholar 

  • Martinez-Alonso M, Vera A, Villaverde A (2007) Role of the chaperone DnaK in protein solubility and conformational quality in inclusion body-forming Escherichia coli cells. FEMS Microbiol Lett 273(2):187–95

    PubMed  CAS  Google Scholar 

  • Martinez-Alonso M, Gonz’alez-Montalb’an N, Garcia-Fruit’os E, Villaverde A. (2008) The functional quality of soluble recombinant polypeptides produced in Escherichia coil is defined by a wide conformational spectrum. Appl Environ Microbiol 74(23):7431–3

    Google Scholar 

  • Matagne A, Dobson CM (1998) The folding process of hen lysozyme: a perspective from the ‘new view’. Cell Mol Life Sci 54(4):363–71

    PubMed  CAS  Google Scholar 

  • Matouschek A (2003) Protein unfolding–an important process in vivo? Curr Opin Struct Biol 13(1):98–109

    Google Scholar 

  • Matuszewska M, Kuczynska-Wisnik D, Laskowska E et al. (2005) The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem 280(13):12292–8

    PubMed  CAS  Google Scholar 

  • Maurizi MR (1992) Proteases and protein degradation in Escherichia coli. Experientia 48(2): 178–201

    PubMed  CAS  Google Scholar 

  • Middelberg AP (2002) Preparative protein refolding. Trends Biotechnol 20(10):437–43

    PubMed  CAS  Google Scholar 

  • Miot M, Betton JM (2004) Protein quality control in the bacterial periplasm. Microb Cell Fact 3(1):4

    PubMed  Google Scholar 

  • Missiakas D, Schwager F, Betton JM et al. (1996) Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. Embo J 15(24):6899–909

    PubMed  CAS  Google Scholar 

  • Mogk A, Bukau B (2004) Molecular chaperones: structure of a protein disaggregase. Curr Biol 14(2):R78–80

    PubMed  CAS  Google Scholar 

  • Mogk A, Deuerling E, Vorderwulbecke S et al. (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50(2):585–95

    PubMed  CAS  Google Scholar 

  • Mogk A, Tomoyasu T, Goloubinoff P et al. (1999) Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. Embo J 18(24): 6934–49

    PubMed  CAS  Google Scholar 

  • Morell M, Bravo R, Espargaro A et al. (2008): Inclusion bodies: Specificity in their aggregation process and amyloid-like structure. Biochim Biophys Acta 1783(10):1815–25

    Google Scholar 

  • Morita MT, Kanemori M, Yanagi H et al. (2000) Dynamic interplay between antagonistic pathways controlling the sigma 32 level in Escherichia coli. Proc Natl Acad Sci U S A 97(11):5860–5

    PubMed  CAS  Google Scholar 

  • Motohashi K, Watanabe Y, Yohda M et al. (1999) Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc Natl Acad Sci USA 96(13):7184–9

    PubMed  CAS  Google Scholar 

  • Muchowski PJ, Schaffar G, Sittler A et al. (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97(14):7841–6

    PubMed  CAS  Google Scholar 

  • Mujacic M, Bader MW, Baneyx F (2004) Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK-DnaJ-GrpE system in the management of protein misfolding under severe stress conditions. Mol Microbiol 51(3):849–59

    PubMed  CAS  Google Scholar 

  • Muramatsu N, Minton AP (1988) Tracer diffusion of globular proteins in concentrated protein solutions. Proc Natl Acad Sci USA 85(9):2984–8

    PubMed  CAS  Google Scholar 

  • Nagai H, Yuzawa H, Kanemori M et al. (1994) A distinct segment of the sigma 32 polypeptide is involved in DnaK-mediated negative control of the heat shock response in Escherichia coli. Proc Natl Acad Sci USA 91(22):10280–4

    PubMed  CAS  Google Scholar 

  • Nahalka J (2008) Physiological aggregation of maltodextrin phosphorylase from Pyrococcus furiosus and its application in a process of batch starch degradation to alpha-D-glucose-1-phosphate. J Ind Microbiol Biotechnol 35(4):219–23

    PubMed  CAS  Google Scholar 

  • Nahalka J, Gemeiner P, Bucko M et al. (2006) Bioenergy beads: a tool for regeneration of ATP/NTP in biocatalytic synthesis. Artif Cells Blood Substit Immobil Biotechnol 34(5):515–21

    PubMed  CAS  Google Scholar 

  • Nahalka J, Nidetzky B (2007) Fusion to a pull-down domain: a novel approach of producing Trigonopsis variabilisD-amino acid oxidase as insoluble enzyme aggregates. Biotechnol Bioeng 97(3):454–61

    PubMed  CAS  Google Scholar 

  • Nahalka J, Vikartovska A, Hrabarova E (2008) A crosslinked inclusion body process for sialic acid synthesis. J Biotechnol 134(1–2):146–53

    Google Scholar 

  • Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66(1):64–93; table of contents

    PubMed  CAS  Google Scholar 

  • Neidhardt FC, Umbarger HE (1996) Chemical composition of Escherichia coli. In: (ed) Escherichia coli and Salmonella, American Society for Microbiology Press, Washington, D.C.

    Google Scholar 

  • Neubauer A, Soini J, Bollok M et al. (2007) Fermentation process for tetrameric human collagen prolyl 4-hydroxylase in Escherichia coli: improvement by gene optimisation of the PDI/beta subunit and repeated addition of the inducer anhydrotetracycline. J Biotechnol 128(2):308–21

    PubMed  CAS  Google Scholar 

  • Niiranen L, Espelid S, Karlsen CR et al. (2007) Comparative expression study to increase the solubility of cold adapted Vibrio proteins in Escherichia coli. Protein Expr Purif 52(1):210–8

    PubMed  CAS  Google Scholar 

  • Nishihara K, Kanemori M, Kitagawa M et al. (1998) Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl Environ Microbiol 64(5):1694–9

    PubMed  CAS  Google Scholar 

  • Nishihara K, Kanemori M, Yanagi H et al. (2000) Overexpression of trigger factor prevents aggregation of recombinant proteins in Escherichia coli. Appl Environ Microbiol 66(3):884–9

    PubMed  CAS  Google Scholar 

  • Oberg K, Chrunyk BA, Wetzel R et al. (1994) Nativelike secondary structure in interleukin-1 beta inclusion bodies by attenuated total reflectance FTIR. Biochemistry 33(9):2628–34

    PubMed  CAS  Google Scholar 

  • Otzen DE, Fersht AR (1998) Folding of circular and permuted chymotrypsin inhibitor 2: retention of the folding nucleus. Biochemistry 37(22):8139–46

    PubMed  CAS  Google Scholar 

  • Panchenko AR, Luthey-Schulten Z, Wolynes PG (1996) Foldons, protein structural modules, and exons. Proc Natl Acad Sci USA 93(5):2008–13

    PubMed  CAS  Google Scholar 

  • Parsell DA, Kowal AS, Singer MA et al. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372(6505):475–8

    PubMed  CAS  Google Scholar 

  • Paul DC, Van Frank RM, Muth WL et al. (1983) Immunocytochemical demonstration of human proinsulin chimeric polypeptide within cytoplasmic inclusion bodies of Escherichia coli. Eur J Cell Biol 31(2):171–4

    PubMed  CAS  Google Scholar 

  • Plakoutsi G, Bemporad F, Calamai M et al. (2005) Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates. J Mol Biol 351(4):910–22

    PubMed  CAS  Google Scholar 

  • Proudfoot AE, Goffin L, Payton MA et al. (1996) In vivo and in vitro folding of a recombinant metalloenzyme, phosphomannose isomerase. Biochem J 318 (Pt 2):437–42

    Google Scholar 

  • Przybycien TM, Dunn JP, Valax P et al. (1994) Secondary structure characterization of beta-lactamase inclusion bodies. Protein Eng 7(1):131–6

    PubMed  CAS  Google Scholar 

  • Rajan RS, Illing ME, Bence NF et al. (2001) Specificity in intracellular protein aggregation and inclusion body formation. Proc Natl Acad Sci USA 98(23):13060–5

    PubMed  CAS  Google Scholar 

  • Ranson NA, Farr GW, Roseman AM et al. (2001) ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107(7):869–79

    PubMed  CAS  Google Scholar 

  • Rinas U, Bailey JE (1992) Protein compositional analysis of inclusion bodies produced in recombinant Escherichia coli. Appl Microbiol Biotechnol 37(5):609–14

    PubMed  CAS  Google Scholar 

  • Rinas U, Bailey JE (1993) Overexpression of bacterial hemoglobin causes incorporation of pre-beta-lactamase into cytoplasmic inclusion bodies. Appl Environ Microbiol 59(2):561–6

    PubMed  CAS  Google Scholar 

  • Rinas U, Boone TC, Bailey JE (1993) Characterization of inclusion bodies in recombinant Escherichia coli producing high levels of porcine somatotropin. J Biotechnol 28(2–3):313–20

    PubMed  CAS  Google Scholar 

  • Rinas U, Hoffmann F, Betiku E et al. (2007) Inclusion body anatomy and functioning of chaperone-mediated in vivo inclusion body disassembly during high-level recombinant protein production in Escherichia coli. J Biotechnol 127(2):244–57

    PubMed  CAS  Google Scholar 

  • Rosen R, Biran D, Gur E et al. (2002) Protein aggregation in Escherichia coli: role of proteases. FEMS Microbiol Lett 207(1):9–12

    PubMed  CAS  Google Scholar 

  • Rudolph R, Lilie H (1996) In vitro folding of inclusion body proteins. Faseb J 10(1):49–56

    PubMed  CAS  Google Scholar 

  • Sahdev S, Khattar SK, Saini KS (2008) Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 307(1–2):249–64

    PubMed  CAS  Google Scholar 

  • Sakikawa C, Taguchi H, Makino Y et al. (1999) On the maximum size of proteins to stay and fold in the cavity of GroEL underneath GroES. J Biol Chem 274(30):21251–6

    PubMed  CAS  Google Scholar 

  • Sastry MS, Korotkov K, Brodsky Y et al. (2002) Hsp31, the Escherichia coli yedU gene product, is a molecular chaperone whose activity is inhibited by ATP at high temperatures. J Biol Chem 277(48):46026–34

    PubMed  CAS  Google Scholar 

  • Schein CH, Noteborn (1988) Formation of soluble recombinant proteins in Escherichia coli is favored by lower growth temperature. Bio/Technology 6(3):291–294

    Google Scholar 

  • Schirmer EC, Glover JR, Singer MA et al. (1996) HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 21(8):289–96

    PubMed  CAS  Google Scholar 

  • Schlieker C, Tews I, Bukau B et al. (2004) Solubilization of aggregated proteins by ClpB/DnaK relies on the continuous extraction of unfolded polypeptides. FEBS Lett 578(3):351–6

    PubMed  CAS  Google Scholar 

  • Schmidt M, Babu KR, Khanna N et al. (1999) Temperature-induced production of recombinant human insulin in high-cell density cultures of recombinant Escherichia coli. J Biotechnol 68(1):71–83

    PubMed  CAS  Google Scholar 

  • Schoemaker JM, Brasnett AH, Marston FA (1985) Examination of calf prochymosin accumulation in Escherichia coli: disulphide linkages are a structural component of prochymosin-containing inclusion bodies. Embo J 4(3):775–80

    PubMed  CAS  Google Scholar 

  • Schoner RG, Ellis LF, Schoner BE (1985) Isolation and purification of protein granules from Escherichia coli cells overproducing bovine growth hormone. Bio/Technology 3:151–154

    CAS  Google Scholar 

  • Schrodel A, de Marco A (2005) Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem 6:10

    PubMed  Google Scholar 

  • Schultz T, Martinez L, de Marco A (2006) The evaluation of the factors that cause aggregation during recombinant expression in E. coli is simplified by the employment of an aggregation-sensitive reporter. Microb Cell Fact 5:28

    PubMed  Google Scholar 

  • Shearstone JR, Baneyx F (1999) Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J Biol Chem 274(15):9937–45

    PubMed  CAS  Google Scholar 

  • Snow CD, Nguyen H, Pande VS et al. (2002) Absolute comparison of simulated and experimental protein-folding dynamics. Nature 420(6911):102–6

    PubMed  CAS  Google Scholar 

  • Sorensen HP, Mortensen KK (2005a) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115(2):113–28

    PubMed  CAS  Google Scholar 

  • Sorensen HP, Mortensen KK (2005b) Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb Cell Fact 4(1):1

    PubMed  Google Scholar 

  • Speed MA, Wang DI, King J (1996) Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat Biotechnol 14(10):1283–7

    PubMed  CAS  Google Scholar 

  • Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97(3):339–47

    PubMed  CAS  Google Scholar 

  • Stefani M, Dobson CM (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 81(11):678–99

    PubMed  CAS  Google Scholar 

  • Straus DB, Walter WA, Gross CA (1987) The heat shock response of E. coli is regulated by changes in the concentration of sigma 32. Nature 329(6137):348–51

    PubMed  CAS  Google Scholar 

  • Sugrue R, Marston FA, Lowe PA et al. (1990) Denaturation studies on natural and recombinant bovine prochymosin (prorennin). Biochem J 271(2):541–7

    PubMed  CAS  Google Scholar 

  • Surewicz WK, Mantsch HH (1988) New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim Biophys Acta 952(2):115–30

    PubMed  CAS  Google Scholar 

  • Surewicz WK, Stepanik TM, Szabo AG et al. (1988) Lipid-induced changes in the secondary structure of snake venom cardiotoxins. J Biol Chem 263(2):786–90

    PubMed  CAS  Google Scholar 

  • Teter SA, Houry WA, Ang D et al. (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97(6):755–65

    PubMed  CAS  Google Scholar 

  • Thomas JG, Ayling A, Baneyx F (1997) Molecular chaperones, folding catalysts, and the recovery of active recombinant proteins from E. coli. To fold or to refold. Appl Biochem Biotechnol 66(3):197–238

    PubMed  CAS  Google Scholar 

  • Thomas JG, Baneyx F (1996a) Protein folding in the cytoplasm of Escherichia coli: requirements for the DnaK-DnaJ-GrpE and GroEL-GroES molecular chaperone machines. Mol Microbiol 21(6):1185–96

    PubMed  CAS  Google Scholar 

  • Thomas JG, Baneyx F (1996b) Protein misfolding and inclusion body formation in recombinant Escherichia coli cells overexpressing Heat-shock proteins. J Biol Chem 271(19):11141–7

    PubMed  CAS  Google Scholar 

  • Thomas JG, Baneyx F (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG In vivo. J Bacteriol 180(19):5165–72

    PubMed  CAS  Google Scholar 

  • Thomas JG, Baneyx F (2000) ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol Microbiol 36(6):1360–70

    PubMed  CAS  Google Scholar 

  • Tokatlidis K, Dhurjati P, Millet J et al. (1991) High activity of inclusion bodies formed in Escherichia coli overproducing Clostridium thermocellum endoglucanase D. FEBS Lett 282(1):205–8

    PubMed  CAS  Google Scholar 

  • Tomoyasu T, Arsene F, Ogura T et al. (2001a) The C terminus of sigma(32) is not essential for degradation by FtsH. J Bacteriol 183(20):5911–7

    PubMed  CAS  Google Scholar 

  • Tomoyasu T, Mogk A, Langen H et al. (2001b) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40(2):397–413

    PubMed  CAS  Google Scholar 

  • Tomoyasu T, Ogura T, Tatsuta T et al. (1998) Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Mol Microbiol 30(3):567–81

    PubMed  CAS  Google Scholar 

  • Tsumoto K, Umetsu M, Kumagai I et al. (2003) Solubilization of active green fluorescent protein from insoluble particles by guanidine and arginine. Biochem Biophys Res Commun 312(4):1383–6

    PubMed  CAS  Google Scholar 

  • Umetsu M, Tsumoto K, Ashish K et al. (2004) Structural characteristics and refolding of in vivo aggregated hyperthermophilic archaeon proteins. FEBS Lett 557(1–3):49–56

    PubMed  CAS  Google Scholar 

  • Umetsu M, Tsumoto K, Nitta S et al. (2005) Nondenaturing solubilization of beta2 microglobulin from inclusion bodies by L-arginine. Biochem Biophys Res Commun 328(1):189–97

    PubMed  CAS  Google Scholar 

  • Vallejo LF, Rinas U (2004) Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 3(1):11

    PubMed  Google Scholar 

  • Veinger L, Diamant S, Buchner J et al. (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273(18):11032–7

    PubMed  CAS  Google Scholar 

  • Vendruscolo M, Paci E, Dobson CM et al. (2003) Rare fluctuations of native proteins sampled by equilibrium hydrogen exchange. J Am Chem Soc 125(51):15686–7

    PubMed  CAS  Google Scholar 

  • Ventura S (2005) Sequence determinants of protein aggregation: tools to increase protein solubility. Microb Cell Fact 4(1):11

    PubMed  Google Scholar 

  • Ventura S, Villaverde A (2006) Protein quality in bacterial inclusion bodies. Trends Biotechnol 24(4):179–85

    PubMed  CAS  Google Scholar 

  • Ventura S, Zurdo J, Narayanan S et al. (2004) Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc Natl Acad Sci USA 101(19):7258–63

    PubMed  CAS  Google Scholar 

  • Vera A, Aris A, Carrio M et al. (2005) Lon and ClpP proteases participate in the physiological disintegration of bacterial inclusion bodies. J Biotechnol 119(2):163–71

    PubMed  CAS  Google Scholar 

  • Vera A, Gonzalez-Montalban N, Aris A et al. (2007) The conformational quality of insoluble recombinant proteins is enhanced at low growth temperatures. Biotechnol Bioeng 96(6):1101–6

    PubMed  CAS  Google Scholar 

  • Villaverde A, Carrio MM (2003) Protein aggregation in recombinant bacteria: biological role of inclusion bodies. Biotechnol Lett 25(17):1385–95

    PubMed  CAS  Google Scholar 

  • Wagner S, Baars L, Ytterberg AJ et al. (2007) Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics 6(9):1527–50

    PubMed  CAS  Google Scholar 

  • Waldo GS, Standish BM, Berendzen J et al. (1999) Rapid protein-folding assay using green fluorescent protein. Nat Biotechnol 17(7):691–5

    PubMed  CAS  Google Scholar 

  • Walsh G (2005) Therapeutic insulins and their large-scale manufacture. Appl Microbiol Biotechnol 67(2):151–9

    PubMed  CAS  Google Scholar 

  • Wang L, Maji SK, Sawaya MR et al. (2008): Bacterial inclusion bodies contain amyloid-like strucure. PLoS Biol 6(8):e195

    Google Scholar 

  • Chan HY, Gray-Board GL et al. (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23(4):425–8

    PubMed  Google Scholar 

  • Wickner S, Gottesman S, Skowyra D et al. (1994) A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci USA 91(25):12218–22

    PubMed  CAS  Google Scholar 

  • Wickner S, Maurizi MR, Gottesman S (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286(5446):1888–93

    PubMed  CAS  Google Scholar 

  • Williams DC, Van Frank RM, Muth WL et al. (1982) Cytoplasmic inclusion bodies in Escherichia coli producing biosynthetic human insulin proteins. Science 215(4533):687–9

    PubMed  CAS  Google Scholar 

  • Wolynes PG, Onuchic JN, Thirumalai D (1995) Navigating the folding routes. Science 267(5204):1619–20

    PubMed  CAS  Google Scholar 

  • Worrall DM, Goss NH (1989) The formation of biologically active beta-galactosidase inclusion bodies in Escherichia coli. Aust J Biotechnol 3(1):28–32

    PubMed  CAS  Google Scholar 

  • Yokoyama K, Kikuchi Y, Yasueda H (1998) Overproduction of DnaJ in Escherichia coli improves in vivo solubility of the recombinant fish-derived transglutaminase. Biosci Biotechnol Biochem 62(6):1205–10

    PubMed  CAS  Google Scholar 

  • Yon JM (2001) Protein folding: a perspective for biology, medicine and biotechnology. Braz J Med Biol Res 34(4):419–35

    PubMed  CAS  Google Scholar 

  • Young JC, Agashe VR, Siegers K et al. (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5(10):781–91

    PubMed  CAS  Google Scholar 

  • Yura T, Nakahigashi K (1999) Regulation of the heat-shock response. Curr Opin Microbiol 2(2):153–8

    PubMed  CAS  Google Scholar 

  • Zhang YB, Howitt J, McCorkle S et al. (2004) Protein aggregation during overexpression limited by peptide extensions with large net negative charge. Protein Expr Purif 36(2):207–16

    PubMed  CAS  Google Scholar 

  • Zhu X, Zhao X, Burkholder WF et al. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272(5268):1606–14

    PubMed  CAS  Google Scholar 

  • Zimmerman SB, Minton AP (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22:27–65

    PubMed  CAS  Google Scholar 

  • Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222(3):599–620

    PubMed  CAS  Google Scholar 

  • Zolkiewski M (1999) ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J Biol Chem 274(40):28083–6

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Biotecnologia i de Biomedicina, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, 08193 Spain

    Antonio Villaverde

Authors
  1. Elena Garcìa-Fruitòs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nuria Gonzàlez-Montalbàn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mònica Martìnez-Alonso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ursula Rinas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonio Villaverde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antonio Villaverde .

Editor information

Editors and Affiliations

  1. Dept. of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology (KAIST), 335 Gwahangno, Yuseong-gu, Daejeon 305-701, Republic of Korea (South Korea)

    Sang Yup Lee

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Garcìa-Fruitòs, E., Gonzàlez-Montalbàn, N., Martìnez-Alonso, M., Rinas, U., Villaverde, A. (2009). Systems-Level Analysis of Protein Quality in Inclusion Body-Forming Escherichia coli Cells. In: Lee, S.Y. (eds) Systems Biology and Biotechnology of Escherichia coli . Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9394-4_15

Download citation

Publish with us

Policies and ethics

Search

Navigation