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The Roles of GroES as a Co-Chaperone for GroEL

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Networking of Chaperones by Co-Chaperones

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

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Abstract

GroES works with the essential chaperone GroEL to mediate the folding of certain proteins from an unfolded or partially folded state. These two proteins form the only essential chaperone machine in E. coli. Both proteins have seven-fold symmetry. GroES acts by binding to one end of the GroEL complex in the presence of nucleotide. In doing this, it has several roles. It displaces bound substrate protein from GroEL into the folding cavity within the GroEL complex, and caps it while the protein folds. It also helps mediate the allosteric transitions that the GroEL complex undergoes during the course of its reaction cycle. A key part of the GroES co-chaperone is an extended loop of amino-acids that is highly mobile when the protein is free but becomes ordered on binding to GroEL, and the interaction between this mobile loop and GroEL helps define both the strength of the binding and the speed with which the chaperone machine passes through its cycle.

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References

  1. Hemmingsen SM, Woolford C, van der Vies SM et al. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 1988; 333:330–334.

    Article  CAS  PubMed  Google Scholar 

  2. Coates AR, Shinnick TM, Ellis RJ. Chaperonin nomenclature. Mol Microbiol 1993; 8:787.

    Article  CAS  PubMed  Google Scholar 

  3. Friedman DI, Olson ER, Georgopoulos C et al. Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol Rev 1984; 48:299–325.

    CAS  PubMed  Google Scholar 

  4. Tilly K, Murialdo H, Georgopoulos C. Identification of a second Escherichia coli groE gene whose product is necessary for bacteriophage morphogenesis. Proc Natl Acad Sci USA 1981; 78:1629–1633.

    Article  CAS  PubMed  Google Scholar 

  5. Hohn T, Hohn B, Engel A et al. Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J Mol Biol 1979; 129:359–373.

    Article  CAS  PubMed  Google Scholar 

  6. Chandrasekhar GN, Tilly K, Woolford C et al. Purification and properties of the groES morphogenetic protein of Escherichia coli. J Biol Chem 1986; 261:12414–12419.

    CAS  PubMed  Google Scholar 

  7. 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.

    CAS  PubMed  Google Scholar 

  8. Zhou YN, Kusukawa N, Erickson JW et al. Isolation and characterization of Escherichia coli mutants that lack the heat shock sigma factor sigma 32. J Bacteriol 1988; 170:3640–3649.

    CAS  PubMed  Google Scholar 

  9. Tilly K, Georgopoulos C. Evidence that the two Escherichia coli groE morphogenetic gene products interact in vivo. J Bacteriol 1982; 149:1082–1088.

    CAS  PubMed  Google Scholar 

  10. Anfinsen CB. Principles that govern the folding of protein chains. Science 1973; 181:223–230.

    Article  CAS  PubMed  Google Scholar 

  11. Goloubinoff P, Gatenby AA, Lorimer GH. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 1989; 337:44–47.

    Article  CAS  PubMed  Google Scholar 

  12. Ellis RJ. Molecular chaperones. Opening and closing the Anfinsen cage. Curr Biol 1994; 4:633–635.

    Article  CAS  PubMed  Google Scholar 

  13. Kerner MJ, Naylor DJ, Ishihama Y et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 2005; 122:209–220.

    Article  CAS  PubMed  Google Scholar 

  14. Goloubinoff P, Christeller JT, Gatenby AA et al. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP. Nature 1989; 342:884–889.

    Article  CAS  PubMed  Google Scholar 

  15. Viitanen PV, Lubben TH, Reed J et al. Chaperonin-facilitated refolding of ribulosebisphosphate carboxylase and ATP hydrolysis by chaperonin 60 (groEL) are K+ dependent. Biochemistry 1990; 29:5665–5671.

    Article  CAS  PubMed  Google Scholar 

  16. Martin J, Langer T, Boteva R et al. Chaperonin-mediated protein folding at the surface of groEL through a ‘molten globule’-like intermediate. Nature 1991; 352:36–42.

    Article  CAS  PubMed  Google Scholar 

  17. Buchner J, Schmidt M, Fuchs M et al. GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 1991; 30:1586–1591.

    Article  CAS  PubMed  Google Scholar 

  18. Mendoza JA, Rogers E, Lorimer GH et al. Chaperonins facilitate the in vitro folding of monomeric mitochondrial rhodanese. Biol Chem 1991; 266:13044–1309.

    CAS  Google Scholar 

  19. Kubo T, Mizobata T, Kawata Y. Refolding of yeast enolase in the presence of the chaperonin GroE: The nucleotide specificity of GroE and the role of GroES. J Biol Chem 1993; 268:19346–19351.

    CAS  PubMed  Google Scholar 

  20. Fisher MT. The effect of groES on the groEL-dependent assembly of dodecameric glutamine synthetase in the presence of ATP and ADP. J Biol Chem 1994; 269:13629–13636.

    CAS  PubMed  Google Scholar 

  21. Schmidt M, Buchner J, Todd MJ et al. On the role of groES in the chaperonin-assisted folding reaction. Three case studies. J Biol Chem 1994; 269:10304–10311.

    CAS  PubMed  Google Scholar 

  22. Hendrix RW. Purification and properties of groE, a host protein involved in bacteriophage assembly. J Mol Biol 1979; 129:375–392.

    Article  CAS  PubMed  Google Scholar 

  23. Hohn T, Hohn B, Engel A et al. Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J Mol Biol 1979; 129:359–373.

    Article  CAS  PubMed  Google Scholar 

  24. Saibil H, Dong Z, Wood S et al. Binding of chaperonins. Nature 1991; 353:25–26.

    Article  CAS  PubMed  Google Scholar 

  25. Chen S, Roseman AM, Hunter AS et al. Location of a folding protein and shape changes in GroEL/GroES complexes imaged by cryo-electron microscopy. Nature 1994; 371:261–264.

    Article  CAS  PubMed  Google Scholar 

  26. Roseman AM, Chen S, White H et al. The chaperonin ATPase cycle: Mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 1996; 87:241–51.

    Article  CAS  PubMed  Google Scholar 

  27. Roseman AM, Ranson NA, Gowen B et al. Structures of unliganded and ATP-bound states of the Escherichia coli chaperonin GroEL by cryoelectron microscopy. J Struct Biol 2001; 135:115–25.

    Article  CAS  PubMed  Google Scholar 

  28. Ranson NA, Farr GW, Roseman AM et al. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 2001; 107:869–879.

    Article  CAS  PubMed  Google Scholar 

  29. Braig K, Otwinowski Z, Hegde R et al. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 1994; 371:578–586.

    Article  CAS  PubMed  Google Scholar 

  30. Boisvert DC, Wang J, Otwinowski Z et al. The 2.4 Å crystal structure of the bacterial chaperonin GroEL complexed with ATP-γ-S. Nat Struct Biol 1996; 3:170–7.

    Article  CAS  PubMed  Google Scholar 

  31. Hunt JF, Weaver AJ, Landry SJ et al. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature 1996; 379:37–45.

    Article  CAS  PubMed  Google Scholar 

  32. Xu Z, Horwich AL, Sigler PB. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 1997; 388:741–50.

    Article  CAS  PubMed  Google Scholar 

  33. Fiaux J, Bertelsen EB, Horwich AL et al. NMR analysis of a 900K GroEL GroES complex. Nature 2002; 418:207–11.

    Article  CAS  PubMed  Google Scholar 

  34. Fenton WA, Kashi Y, Furtak K et al. Residues in chaperonin GroEL required for polypeptide binding and release. Nature 1994; 371:614–619.

    Article  CAS  PubMed  Google Scholar 

  35. Landry SJ, Zeilstra-Ryalls J, Fayet O et al. Characterization of a functionally important mobile domain of GroES. Nature 1993; 364:255–8.

    Article  CAS  PubMed  Google Scholar 

  36. Shewmaker F, Maskos K, Simmerling C et al. The disordered mobile loop of GroES folds into a defined beta-hairpin upon binding GroEL. J Biol Chem 2001; 276:31257–64.

    Article  CAS  PubMed  Google Scholar 

  37. Kovalenko O, Yifrach O, Horovitz A. Residue lysine-34 in GroES modulates allosteric transitions in GroEL. Biochemistry 1994; 33:14974–8.

    Article  CAS  PubMed  Google Scholar 

  38. Torok Z, Vigh L, Goloubinoff P. Fluorescence detection of symmetric GroELl4(GroES7)2 hetero-oligomers involved in protein release during the chaperonin cycle. J Biol Chem 1996; 271:16180–16186.

    Article  CAS  PubMed  Google Scholar 

  39. Azem A, Diamant S, Kessel M et al. The protein-folding activity of chaperonins correlates with the symmetric GroELl4(GroES7)2 hetero-oligomer. Proc Natl Acad Sci USA 1995; 92:12021–12025.

    Article  CAS  PubMed  Google Scholar 

  40. Diamant S, Azem A, Weiss C et al. Increased efficiency of GroE-assisted protein folding by manganese ions. J Biol Chem 1995; 270:28387–28391.

    Article  CAS  PubMed  Google Scholar 

  41. Mayhew M, da Silva AC, Martin J et al. Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 1996; 379:420–426.

    Article  CAS  PubMed  Google Scholar 

  42. Brinker A, Pfeifer G, Kerner MJ et al. Dual function of protein confinement in chaperonin-assisted protein folding. Cell 2001; 107:223–233.

    Article  CAS  PubMed  Google Scholar 

  43. Ranson NA, White HE, Saibil HR. Chaperonins. Biochem J 1998; 333:233–242.

    CAS  PubMed  Google Scholar 

  44. Richardson A, Landry SJ, Georgopoulos C. The ins and outs of a molecular chaperone machine. Trends Biochem Sci 1998; 23:138–43.

    Article  CAS  PubMed  Google Scholar 

  45. Sigler PB, Xu Z, Rye HS et al. Structure and function in GroEL-mediated protein folding. Annu Rev Biochem 1998; 67:581–608.

    Article  CAS  PubMed  Google Scholar 

  46. Wang JD, Weissman JS. Thinking outside the box: New insights into the mechanism of GroEL-mediated protein folding. Nat Struct Biol 1999; 6:597–600.

    Article  CAS  PubMed  Google Scholar 

  47. Weissman JS, Rye HS, Fenton WA et al. Characterisation of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 1996; 84:481–490.

    Article  CAS  PubMed  Google Scholar 

  48. Weissman JS, Hohl CM, Kovalenko O et al. Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under GroES. Cell 1995; 83:577–587.

    Article  CAS  PubMed  Google Scholar 

  49. Rye HS, Burston SG, Fenton WA et al. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 1997; 388:792–798.

    Article  CAS  PubMed  Google Scholar 

  50. Rye HS, Roseman AM, Chen S et al. GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 1999; 97:325–338.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  52. Lorimer G. Protein folding. Folding with a two-stroke motor. Nature 1997; 388:723.

    Article  Google Scholar 

  53. Houry WA, Frishman D, Eckerskorn C et al. Identification of in vivo substrates of the chaperonin GroEL. Nature 1999; 402:147–154.

    Article  CAS  PubMed  Google Scholar 

  54. Wang JD, Herman C, Tipton KA et al. Directed evolution of substrate-optimized GroEL/S chaperonins. Cell 2002; 111:1027–1039.

    Article  CAS  PubMed  Google Scholar 

  55. Todd MJ, Viitanen PV, Lorimer GH. Dynamics of the chaperonin ATPase cycle: Implications for facilitated protein folding. Science 1994; 265:659–66.

    Article  CAS  PubMed  Google Scholar 

  56. Horovitz A, Fridmann Y, Kafri G et al. Allostery in chaperonins. J Struct Biol 2001; 135:104–114.

    Article  CAS  PubMed  Google Scholar 

  57. Viitanen PV, Gatenby AA, Lorimer GH. Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci 1992; 1:363–9.

    CAS  PubMed  Google Scholar 

  58. Gordon CL, Sather SK, Casjens S et al. Selective in vivo rescue by GroEL/ES of thermolabile folding intermediates to phage P22 structural proteins. J Biol Chem 1994; 269:27941–51.

    CAS  PubMed  Google Scholar 

  59. Brunschier R, Danner M, Seckler R. Interactions of phage P22 tailspike protein with GroE molecular chaperones during refolding in vitro. J Biol Chem 1993; 268:2767–72.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  61. Chaudhuri TK, Farr GW, Fenton WA et al. GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 2001; 107:235–46.

    Article  CAS  PubMed  Google Scholar 

  62. Farr GW, Fenton WA, Chaudhuri TK et al. Folding with and without encapsulation by cis-and trans-only GroEL-GroES complexes. EMBO J 2003; 22:3220–30.

    Article  CAS  PubMed  Google Scholar 

  63. Laemmli UK, Geguin F, Gujer-Kellenberger G. A factor preventing the major head protein of bacteriophage T4 from random aggregation. J Mol Biol 1970; 47:69–85.

    Article  CAS  PubMed  Google Scholar 

  64. Georgopoulos CP, Hendrix RW, Kaiser AD et al. Role of the host cell in bacteriophage morphogenesis: Effects of a bacterial mutation on T4 head assembly. Nature New Biol 1972; 239:38–41.

    Article  CAS  PubMed  Google Scholar 

  65. Takano T, Kakefuda T. Involvement of a bacterial factor in morphogenesis of bacteriophage capsid. Nature New Biol 1972; 239:34–37.

    Article  CAS  PubMed  Google Scholar 

  66. van der Vies SM, Gatenby AA et al. Bacteriophage T4 encodes a co-chaperonin that can substitute for Escherichia coli GroES in protein folding. Nature 1994; 368:654–656.

    Article  PubMed  Google Scholar 

  67. Keppel F, Rychner M, Georgopoulos C. Bacteriophage-encoded co-chaperonins can substitute for Escherichia coli’s essential GroES protein. EMBO reports 2002; 3:893–898.

    Article  CAS  PubMed  Google Scholar 

  68. Hunt JF, van der Vies SM, Henry L et al. Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage. Cell 1997; 90:361–371.

    Article  CAS  PubMed  Google Scholar 

  69. Bakkes PJ, Faber BW, van Heerikhuizen H et al. The T4-encoded co-chaperonin, gp31, has unique properties that explain its requirement for the folding of the T4 major capsid protein. Proc Natl Acad Sci USA 2005; 102:8144–8149.

    Article  CAS  PubMed  Google Scholar 

  70. Viitanen PV, Lorimer GH, Seetheram R et al. Mammalian mitochondrial chaperonin 60 functions as a single toroidal ring. J Biol Chem 1992; 267:695–698.

    CAS  PubMed  Google Scholar 

  71. Nielsen KL, Cowan NJ. A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol Cell 1998; 2:93–100.

    Article  CAS  PubMed  Google Scholar 

  72. Levy-Rimler G, Viitanen P, Weiss C et al. The effect of nucleotides and mitochondrial chaperonin 10 on the structure and chaperone activity of mitochondrial chaperonin 60. Europ J Biochem 2001; 268:3465–3472.

    Article  CAS  PubMed  Google Scholar 

  73. Richardson A, Schwager F, Landry SJ et al. The importance of a mobile loop in regulating chaperonin/ co-chaperonin interaction: Humans versus Escherichia coli. J Biol Chem 2001; 276:4981–4987.

    Article  CAS  PubMed  Google Scholar 

  74. Shewmaker F, Kerner MJ, Hayer-Hartl M et al. A mobile loop order-disorder transition modulates the speed of chaperonin cycling. Protein Sci 2004; 13:2139–2148.

    Article  CAS  PubMed  Google Scholar 

  75. Cavanagh AC, Morton H. The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10. Eur J Biochem 1994; 222:551–60.

    Article  CAS  PubMed  Google Scholar 

  76. Sayle R, Milner-White EJ. RasMol: Biomolecular graphics for all. Trends Biochem Sci 1995; 20:374.

    Article  CAS  PubMed  Google Scholar 

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  1. School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK

    Han Liu & Peter A. Lund

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Liu, H., Lund, P.A. (2007). The Roles of GroES as a Co-Chaperone for GroEL. In: Networking of Chaperones by Co-Chaperones. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/978-0-387-49310-7_7

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