Advertisement

Thermophilic Protein Folding Systems

  • Haibin Luo
  • Frank T. Robb

Introduction

The study of adaptive stress responses was initiated at the molecular level with the observation of dramatic chromosome puffs coupled to the inducible transcription of specific proteins that were observed in Drosophila under heat stress (Ritossa 1962). Since then, stress responses have been observed in virtually all classes of organisms. Although a wide variety of survival strategies are deployed when cells are exposed to environmental challenges, such as heat stress, desiccation, chemical stress, or starvation, usually, the effector proteins are generically referred to as Heat Shock Proteins (HSPs). HSPs are diverse in structure and function, and are usually classified based on their subunit molecular weights. Classes that occur in microorganisms and in the majority of thermophiles include HSP100, HSP90, HSP70, HSP60, and the small HSPs (Trent 1996). Most of these proteins function as molecular chaperones, catalyzing the refolding of denatured proteins and assisting the...

Keywords

Archaeal Genome Archaeal Group Penicillin Amidase Methanosarcina Acetivorans Methanocaldococcus Jannaschii 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aivaliotis M, Macek B, Gnad F, Reichelt P, Mann M, Oesterhelt D (2009) Ser/Thr/Tyr protein phosphorylation in the archaeon Halobacterium salinarum–a representative of the third domain of life. PLoS ONE 4(3):e4777PubMedCrossRefGoogle Scholar
  2. Andra S, Frey G, Nitsch M, Baumeister W, Stetter KO (1996) Purification and structural characterization of the thermosome from the hyperthermophilic archaeum Methanopyrus kandleri. FEBS Lett 379(2):127–131PubMedCrossRefGoogle Scholar
  3. Archibald JM, Logsdon JM, Doolittle WF (1999) Recurrent paralogy in the evolution of archaeal chaperonins. Curr Biol 9(18):1053–1056PubMedCrossRefGoogle Scholar
  4. Barber RD, Ferry JG (2001) Archaeal proteasomes. Meth Enzymol 330:413–424PubMedCrossRefGoogle Scholar
  5. Benaroudj N, Zwickl P, Seemuller E, Baumeister W, Goldberg AL (2003) ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol Cell 11(1):69–78PubMedCrossRefGoogle Scholar
  6. Bergeron LM, Gomez L, Whitehead TA, Clark DS (2009) Self-renaturing enzymes: design of an enzyme-chaperone chimera as a new approach to enzyme stabilization. Biotechnol Bioeng 102(5):1316–1322PubMedCrossRefGoogle Scholar
  7. Bigotti MG, Clarke AR (2005) Cooperativity in the thermosome. J Mol Biol 348(1):13–26PubMedCrossRefGoogle Scholar
  8. Blochl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO (1997) Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113°C. Extremophiles 1(1):14–21PubMedCrossRefGoogle Scholar
  9. Boonyaratanakornkit BB, Simpson AJ, Whitehead TA, Fraser CM, El-Sayed NM, Clark DS (2005) Transcriptional profiling of the hyperthermophilic methanarchaeon Methanococcus jannaschii in response to lethal heat and non-lethal cold shock. Environ Microbiol 7(6):789–797PubMedCrossRefGoogle Scholar
  10. Braig K (1998) Chaperonins. Curr Opin Struct Biol 8(2):159–165PubMedCrossRefGoogle Scholar
  11. Brinker A, Pfeifer G, Kerner MJ, Naylor DJ, Hartl FU, Hayer-Hartl M (2001) Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107(2):223–233PubMedCrossRefGoogle Scholar
  12. Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366PubMedCrossRefGoogle Scholar
  13. Cao A, Wang Z, Wei P, Xu F, Cao J, Lai L (2008) Preheating induced homogeneity of the small heat shock protein from Methanococcus jannaschii. Biochim Biophys Acta 1784(3):489–495PubMedCrossRefGoogle Scholar
  14. Cavicchioli R, Thomas T, Curmi PM (2000) Cold stress response in Archaea. Extremophiles 4(6):321–331PubMedCrossRefGoogle Scholar
  15. Ditzel L, Lowe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93(1):125–138PubMedCrossRefGoogle Scholar
  16. Elad N, Farr GW, Clare DK, Orlova EV, Horwich AL, Saibil HR (2007) Topologies of a substrate protein bound to the chaperonin GroEL. Mol Cell 26(3):415–426PubMedCrossRefGoogle Scholar
  17. Emmerhoff OJ, Klenk HP, Birkeland NK (1998) Characterization and sequence comparison of temperature-regulated chaperonins from the hyperthermophilic archaeon Archaeoglobus fulgidus. Gene 215(2):431–438PubMedCrossRefGoogle Scholar
  18. Farr GW, Furtak K, Rowland MB, Ranson NA, Saibil HR, Kirchhausen T, Horwich AL (2000) Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 100(5):561–573PubMedCrossRefGoogle Scholar
  19. Furutani M, Iida T, Yoshida T, Maruyama T (1998) Group II chaperonin in a thermophilic methanogen. Methanococcus thermolithotrophicus. Chaperone activity and filament-forming ability. J Biol Chem 273(43):28399–28407PubMedCrossRefGoogle Scholar
  20. Futterer O, Angelov A, Liesegang H, Gottschalk G, Schleper C, Schepers B, Dock C, Antranikian G, Liebl W (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci USA 101(24):9091–9096PubMedCrossRefGoogle Scholar
  21. Geissler S, Siegers K, Schiebel E (1998) A novel protein complex promoting formation of functional alpha- and gamma-tubulin. EMBO J 17(4):952–966PubMedCrossRefGoogle Scholar
  22. Goloubinoff P, Christeller JT, Gatenby AA, Lorimer GH (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfoleded state depends on two chaperonin proteins and Mg-ATP. Nature 342(6252):884–889PubMedCrossRefGoogle Scholar
  23. Groll M, Clausen T (2003) Molecular shredders: how proteasomes fulfill their role. Curr Opin Struct Biol 13(6):665–673PubMedCrossRefGoogle Scholar
  24. Guagliardi A, Cerchia L, Bartolucci S, Rossi M (1994) The chaperonin from the archaeon Sulfolobus solfataricus promotes correct refolding and prevents thermal denaturation in vitro. Protein Sci 3(9):1436–1443PubMedCrossRefGoogle Scholar
  25. Guagliardi A, Cerchia L, Rossi M (1995) Prevention of in vitro protein thermal aggregation by the Sulfolobus solfataricus chaperonin. Evidence for nonequivalent binding surfaces on the chaperonin molecule. J Biol Chem 270(47):28126–28132PubMedCrossRefGoogle Scholar
  26. Gutsche I, Essen LO, Baumeister W (1999) Group II chaperonins: new TRiC(k)s and turns of a protein folding machine. J Mol Biol 293(2):295–312PubMedCrossRefGoogle Scholar
  27. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295(5561):1852–1858PubMedCrossRefGoogle Scholar
  28. Haslbeck M, Kastenmuller A, Buchner J, Weinkauf S, Braun N (2008) Structural dynamics of archaeal small heat shock proteins. J Mol Biol 378(2):362–374PubMedCrossRefGoogle Scholar
  29. Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89(21):10449–10453PubMedCrossRefGoogle Scholar
  30. Iizuka R, So S, Inobe T, Yoshida T, Zako T, Kuwajima K, Yohda M (2004) Role of the helical protrusion in the conformational change and molecular chaperone activity of the archaeal group II chaperonin. J Biol Chem 279(18):18834–18839PubMedCrossRefGoogle Scholar
  31. Iizuka R, Yoshida T, Ishii N, Zako T, Takahashi K, Maki K, Inobe T, Kuwajima K, Yohda M (2005) Characterization of archeal group II chaperonin-ADP-metal fluoride complexes: ımplications that group II chaperonins operate as a “two-stroke engine”. J Biol Chem 280:40375–40383PubMedCrossRefGoogle Scholar
  32. Iizuka R, Sugano Y, Ide N, Ohtaki A, Yoshida T, Fujiwara S, Imanaka T, Yohda M (2008) Functional characterization of recombinant prefoldin complexes from a hyperthermophilic archaeon, Thermococcus sp. strain KS-1. J Mol Biol 377(3):972–983PubMedCrossRefGoogle Scholar
  33. Izumi M, Fujiwara S, Takagi M, Kanaya S, Imanaka T (1999) Isolation and characterization of a second subunit of molecular chaperonin from Pyrococcus kodakaraensis KOD1: analysis of an ATPase-deficient mutant enzyme. Appl Environ Microbiol 65(4):1801–1805PubMedGoogle Scholar
  34. Izumi M, Fujiwara S, Takagi M, Fukui K, Imanaka T (2001) Two kinds of archaeal chaperonin with different temperature dependency from a hyperthermophile. Biochem Biophys Res Commun 280(2):581–587PubMedCrossRefGoogle Scholar
  35. Jacob U, Gaestel M, Katrin E, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268(3):1517–1520Google Scholar
  36. Kagawa HK, Yaoi T, Brocchieri L, McMillan RA, Alton T, Trent JD (2003) The composition, structure and stability of a group II chaperonin are temperature regulated in a hyperthermophilic archaeon. Mol Microbiol 48(1):143–156PubMedCrossRefGoogle Scholar
  37. Kanzaki T, Ushioku S, Nakagawa A, Oka T, Takahashi K, Nakamura T, Kuwajima K, Yamagishi A, Yohda M (2010) Adaptation of a hyperthermophilic group II chaperonin to relatively moderate temperatures. Protein Eng Des Sel 23:393–402PubMedCrossRefGoogle Scholar
  38. Kida H, Sugano Y, Iizuka R, Fujihashi M, Yohda M, Miki K (2008) Structural and molecular characterization of the prefoldin beta subunit from Thermococcus strain KS-1. J Mol Biol 383(3):465–474PubMedCrossRefGoogle Scholar
  39. Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394(6693):595–599PubMedCrossRefGoogle Scholar
  40. Kim DR, Lee I, Ha SC, Kim KK (2003) Activation mechanism of HSP16.5 from Methanococcus jannaschii. Biochem Biophys Res Commun 307(4):991–998PubMedCrossRefGoogle Scholar
  41. Klumpp M, Baumeister W (1998) The thermosome: archetype of group II chaperonins. FEBS Lett 430(1–2):73–77PubMedCrossRefGoogle Scholar
  42. Klunker D, Haas B, Hirtreiter A, Figueiredo L, Naylor DJ, Pfeifer G, Muller V, Deppenmeier U, Gottschalk G, Hartl FU, Hayer-Hartl M (2003) Coexistence of group I and group II chaperonins in the archaeon Methanosarcina mazei. J Biol Chem 278(35):33256–33267PubMedCrossRefGoogle Scholar
  43. Knapp S, Schmidt-Krey I, Hebert H, Bergman T, Jornvall H, Ladenstein R (1994) The molecular chaperonin TF55 from the Thermophilic archaeon Sulfolobus solfataricus. A biochemical and structural characterization. J Mol Biol 242(4):397–407PubMedGoogle Scholar
  44. Kohda J, Kawanishi H, Suehara K, Nakano Y, Yano T (2006) Stabilization of free and immobilized enzymes using hyperthermophilic chaperonin. J Biosci Bioeng 101(2):131–136PubMedCrossRefGoogle Scholar
  45. Kowalski JM, Kelly RM, Konisky J, Clark DS, Wittrup KD (1998) Purification and functional characterization of a chaperone from Methanococcus jannaschii. Syst Appl Microbiol 21(2):173–178PubMedCrossRefGoogle Scholar
  46. Kusmierczyk AR, Martin J (2003) Nucleotide-dependent protein folding in the type II chaperonin from the mesophilic archaeon Methanococcus maripaludis. Biochem J 371(Pt 3):669–673PubMedCrossRefGoogle Scholar
  47. Laksanalamai P, Maeder DL, Robb FT (2001) Regulation and Mechanism of Action of the Small Heat Shock Protein from the Hyperthermophilic Archaeon Pyrococcus furiosus. J Bacteriol 183(17):5198–5202PubMedCrossRefGoogle Scholar
  48. Laksanalamai P, Pavlov AR, Slesarev AI, Robb FT (2006) Stabilization of Taq DNA polymerase at high temperature by protein folding pathways from a hyperthermophilic archaeon, Pyrococcus furiosus. Biotechnol Bioeng 93(1):1–5PubMedCrossRefGoogle Scholar
  49. Laksanalamai P, Narayan S, Luo H, Robb FT (2009) Chaperone action of a versatile small heat shock protein from Methanococcoides burtonii, a cold adapted archaeon. Proteins 75(2):275–281PubMedCrossRefGoogle Scholar
  50. Large AT, Kovacs E, Lund PA (2002) Properties of the chaperonin complex from the halophilic archaeon Haloferax volcanii. FEBS Lett 532(3):309–312PubMedCrossRefGoogle Scholar
  51. Large AT, Goldberg MD, Lund PA (2009) Chaperones and protein folding in the archaea. Biochem Soc Trans 37(Pt 1):46–51PubMedCrossRefGoogle Scholar
  52. Leroux MR, Fandrich M, Klunker D, Siegers K, Lupas AN, Brown JR, Schiebel E, Dobson CM, Hartl FU (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J 18(23):6730–6743PubMedCrossRefGoogle Scholar
  53. Lin Z, Rye HS (2006) GroEL-mediated protein folding: making the impossible, possible. Crit Rev Biochem Mol Biol 41(4):211–239PubMedCrossRefGoogle Scholar
  54. Liu C, Young AL, Starling-Windhof A, Bracher A, Saschenbrecker S, Rao BV, Rao KV, Berninghausen O, Mielke T, Hartl FU, Beckmann R, Hayer-Hartl M (2010) Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463(7278):197–202PubMedCrossRefGoogle Scholar
  55. Llorca O, Martin-Benito J, Grantham J, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM (2001) The “sequential allosteric ring” mechanism in the eukaryotic chaperonin-assisted folding of actin and tubulin. EMBO J 20(15):4065–4075PubMedCrossRefGoogle Scholar
  56. Lowe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268(5210):533–539PubMedCrossRefGoogle Scholar
  57. Lund PA, Large AT, Kapatai G (2003) The chaperonins: perspectives from the Archaea. Biochem Soc Trans 31(Pt 3):681–685PubMedGoogle Scholar
  58. Lundin VF, Stirling PC, Gomez-Reino J, Mwenifumbo JC, Obst JM, Valpuesta JM, Leroux MR (2004) Molecular clamp mechanism of substrate binding by hydrophobic coiled-coil residues of the archaeal chaperone prefoldin. Proc Natl Acad Sci USA 101(13):4367–4372PubMedCrossRefGoogle Scholar
  59. Luo H, Laksanalamai P, Robb FT (2009) An exceptionally stable Group II chaperonin from the hyperthermophile Pyrococcus furiosus. Arch Biochem Biophys 486(1):12–18PubMedCrossRefGoogle Scholar
  60. Maeder DL, Weiss RB, Dunn DM, Cherry JL, Gonzalez JM, DiRuggiero J, Robb FT (1999) Divergence of the hyperthermophilic archaea Pyrococcus furiosus and P. horikoshii inferred from complete genomic sequences. Genetics 152(4):1299–1305PubMedGoogle Scholar
  61. Marco S, Urena D, Carrascosa JL, Waldmann T, Peters J, Hegerl R, Pfeifer G, Sack-Kongehl H, Baumeister W (1994) The molecular chaperone TF55. Assessment of symmetry. FEBS Lett 341(2–3):152–155PubMedCrossRefGoogle Scholar
  62. Martin-Benito J, Gomez-Reino J, Stirling PC, Lundin VF, Gomez-Puertas P, Boskovic J, Chacon P, Fernandez JJ, Berenguer J, Leroux MR, Valpuesta JM (2007) Divergent substrate-binding mechanisms reveal an evolutionary specialization of eukaryotic prefoldin compared to its archaeal counterpart. Structure 15(1):101–110PubMedCrossRefGoogle Scholar
  63. Maupin-Furlow JA, Gil MA, Karadzic IM, Kirkland PA, Reuter CJ (2004) Proteasomes: perspectives from the Archaea. Front Biosci 9:1743–1758PubMedCrossRefGoogle Scholar
  64. Meyer AS, Walther D, Millet IS, Doniach S, Frydman J (2003) Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113(3):369–381PubMedCrossRefGoogle Scholar
  65. Minuth T, Frey G, Lindner P, Rachel R, Stetter KO, Jaenicke R (1998) Recombinant homo- and hetero-oligomers of an ultrastable chaperonin from the archaeon Pyrodictium occultum show chaperone activity in vitro. Eur J Biochem 258(2):837–845PubMedCrossRefGoogle Scholar
  66. Mitsuzawa S, Kagawa H, Li Y, Chan SL, Paavola CD, Trent JD (2009) The rosettazyme: a synthetic cellulosome. J Biotechnol 143(2):139–144PubMedCrossRefGoogle Scholar
  67. Muchowski PJ, Hays LG, Yates JR 3rd, Clark JI (1999) ATP and the core “alpha-Crystallin” domain of the small heat-shock protein alphaB-crystallin. J Biol Chem 274(42):30190–30195PubMedCrossRefGoogle Scholar
  68. Nakamura N, Taguchi H, Ishii N, Yoshida M, Suzuki M, Endo I, Miura K, Yohda M (1997) Purification and molecular cloning of the group II chaperonin from the acidothermophilic archaeon, Sulfolobus sp. strain 7. Biochem Biophys Res Commun 236(3):727–732PubMedCrossRefGoogle Scholar
  69. Nitsch M, Klumpp M, Lupas A, Baumeister W (1997) The thermosome: alternating alpha and beta-subunits within the chaperonin of the archaeon Thermoplasma acidophilum. J Mol Biol 267:142–149PubMedCrossRefGoogle Scholar
  70. Nitsch M, Walz J, Typke D, Klumpp M, Essen LO, Baumeister W (1998) Group II chaperonin in an open conformation examined by electron tomography. Nat Struct Biol 5(10):855–857PubMedCrossRefGoogle Scholar
  71. Ohtaki A, Kida H, Miyata Y, Ide N, Yonezawa A, Arakawa T, Iizuka R, Noguchi K, Kita A, Odaka M, Miki K, Yohda M (2008) Structure and molecular dynamics simulation of archaeal prefoldin: the molecular mechanism for binding and recognition of nonnative substrate proteins. J Mol Biol 376(4):1130–1141PubMedCrossRefGoogle Scholar
  72. Okochi M, Matsuzaki H, Nomura T, Ishii N, Yohda M (2005) Molecular characterization of the group II chaperonin from the hyperthermophilic archaeum Pyrococcus horikoshii OT3. Extremophiles 9(2):127–134PubMedCrossRefGoogle Scholar
  73. Phipps BM, Hoffmann A, Stetter KO, Baumeister W (1991) A novel ATPase complex selectively accumulated upon heat shock is a major cellular component of thermophilic archaebacteria. EMBO J 10(7):1711–1722PubMedGoogle Scholar
  74. Puhler G, Weinkauf S, Bachmann L, Muller S, Engel A, Hegerl R, Baumeister W (1992) Subunit stoichiometry and three-dimensional arrangement in proteasomes from Thermoplasma acidophilum. EMBO J 11(4):1607–1616PubMedGoogle Scholar
  75. Rechsteiner M, Hoffman L, Dubiel W (1993) The multicatalytic and 26 S proteases. J Biol Chem 268(9):6065–6068PubMedGoogle Scholar
  76. Reimann B, Bradsher J, Franke J, Hartmann E, Wiedmann M, Prehn S, Wiedmann B (1999) Initial characterization of the nascent polypeptide-associated complex in yeast. Yeast 15(5):397–407PubMedCrossRefGoogle Scholar
  77. Ritossa F (1962) A new puffing pattern induced by temperature showck and DNP in Drosophila. Experientia 18:571–573CrossRefGoogle Scholar
  78. Robb FT, Maeder DL (1998) Novel evolutionary histories and adaptive features of proteins from hyperthermophiles. Curr Opin Biotechnol 9(3):288–291PubMedCrossRefGoogle Scholar
  79. Roy SK, Hiyama T, Nakamoto H (1999) Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an alpha-crystallin-related, small heat shock protein. Eur J Biochem 262(2):406–416PubMedCrossRefGoogle Scholar
  80. Ruepp A, Rockel B, Gutsche I, Baumeister W, Lupas AN (2001) The Chaperones of the archaeon Thermoplasma acidophilum. J Struct Biol 135(2):126–138PubMedCrossRefGoogle Scholar
  81. Schoehn G, Hayes M, Cliff M, Clarke AR, Saibil HR (2000a) Domain rotations between open, closed and bullet-shaped forms of the thermosome, an archaeal chaperonin. J Mol Biol 301(2):323–332PubMedCrossRefGoogle Scholar
  82. Schoehn G, Quaite-Randall E, Jimenez JL, Joachimiak A, Saibil HR (2000b) Three conformations of an archaeal chaperonin, TF55 from Sulfolobus shibatae. J Mol Biol 296(3):813–819PubMedCrossRefGoogle Scholar
  83. Shashidharamurthy R, Koteiche HA, Dong J, Mchaourab HS (2005) Mechanism of chaperone function in small heat shock proteins: dissociation of the HSP27 oligomer is required for recognition and binding of destabilized T4 lysozyme. J Biol Chem 280:5281–5289PubMedCrossRefGoogle Scholar
  84. Shomura Y, Yoshida T, Iizuka R, Maruyama T, Yohda M, Miki K (2004) Crystal structures of the group II chaperonin from Thermococcus strain KS-1: steric hindrance by the substituted amino acid, and inter-subunit rearrangement between two crystal forms. J Mol Biol 335(5):1265–1278PubMedCrossRefGoogle Scholar
  85. Siegert R, Leroux MR, Scheufler C, Hartl FU, Moarefi I (2000) Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103(4):621–632PubMedCrossRefGoogle Scholar
  86. Sigler PB, Horwich AL (1995) Unliganded GroEL at 2.8 A: structure and functional implications. Philos Trans R Soc Lond B Biol Sci 348(1323):113–119PubMedCrossRefGoogle Scholar
  87. Spreter T, Pech M, Beatrix B (2005) The crystal structure of archaeal nascent polypeptide-associated complex (NAC) reveals a unique fold and the presence of a ubiquitin-associated domain. J Biol Chem 280(16):15849–15854PubMedCrossRefGoogle Scholar
  88. Stirling PC, Lundin VF, Leroux MR (2003) Getting a grip on non-native proteins. EMBO Rep 4(6):565–570PubMedCrossRefGoogle Scholar
  89. Tamura T, Nagy I, Lupas A, Lottspeich F, Cejka Z, Schoofs G, Tanaka K, De Mot R, Baumeister W (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5(7):766–774PubMedCrossRefGoogle Scholar
  90. Thomas AS, Elcock AH (2004) Molecular simulations suggest protein salt bridges are uniquely suited to life at high temperature. J Am Chem Soc 126:2208–2214PubMedCrossRefGoogle Scholar
  91. Trent JD (1996) A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea. FEMS Microbiol Rev 18(2–3):249–258CrossRefGoogle Scholar
  92. Trent JD, Nimmesgern E, Wall JS, Hartl FU, Horwich AL (1991) A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature 354(6353):490–493PubMedCrossRefGoogle Scholar
  93. Trent JD, Kagawa HK, Yaoi T, Olle E, Zaluzec NJ (1997) Chaperonin filaments: the archaeal cytoskeleton? Proc Natl Acad Sci USA 94(10):5383–5388PubMedCrossRefGoogle Scholar
  94. Usui K, Yoshida T, Maruyama T, Yohda M (2001) Small heat shock protein of a hyperthermophilic archaeum, Thermococcus sp. strain KS-1, exists as a spherical 24 mer and its expression is highly induced under heat-stress conditions. J Biosci Bioeng 92(2):161–166PubMedGoogle Scholar
  95. Vainberg IE, Lewis SA, Rommelaere H, Ampe C, Vandekerckhove J, Klein HL, Cowan NJ (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93(5):863–873PubMedCrossRefGoogle Scholar
  96. Vetriani C, Maeder DL, Tolliday N, Yip KS, Stillman TJ, Britton KL, Rice DW, Klump HH, Robb FT (1998) Protein thermostability above 100°C: a key role for ionic interactions. Proc Natl Acad Sci USA 95(21):12300–12305PubMedCrossRefGoogle Scholar
  97. Waldmann T, Lupas A, Kellermann J, Peters J, Baumeister W (1995) Primary structure of the thermosome from Thermoplasma acidophilum. Biol Chem Hoppe Seyler 376(2):119–126PubMedCrossRefGoogle Scholar
  98. Whitehead TA, Boonyaratanakornkit BB, Hollrigl V, Clark DS (2007) A filamentous molecular chaperone of the prefoldin family from the deep-sea hyperthermophile Methanocaldococcus jannaschii. Protein Sci 16(4):626–634PubMedCrossRefGoogle Scholar
  99. Yan Z, Fujiwara S, Kohda K, Takagi M, Imanaka T (1997) In vitro stabilization and in vivo solubilization of foreign proteins by the beta subunit of a chaperonin from the hyperthermophilic archaeon Pyrococcus sp. strain KOD1. Appl Environ Microbiol 63(2):785–789PubMedGoogle Scholar
  100. Yoshida T, Yohda M, Iida T, Maruyama T, Taguchi H, Yazaki K, Ohta T, Odaka M, Endo I, Kagawa Y (1997) Structural and functional characterization of homo-oligomeric complexes of alpha and beta chaperonin subunits from the hyperthermophilic archaeum Thermococcus strain KS-1. J Mol Biol 273(3):635–645PubMedCrossRefGoogle Scholar
  101. Yoshida T, Ideno A, Hiyamuta S, Yohda M, Maruyama T (2001) Natural chaperonin of the hyperthermophilic archaeum, Thermococcus strain KS-1: a hetero-oligomeric chaperonin with variable subunit composition. Mol Microbiol 39(5):1406–1413PubMedCrossRefGoogle Scholar
  102. Yoshida T, Ideno A, Suzuki R, Yohda M, Maruyama T (2002a) Two kinds of archaeal group II chaperonin subunits with different thermostability in Thermococcus strain KS-1. Mol Microbiol 44(3):761–769PubMedCrossRefGoogle Scholar
  103. Yoshida T, Kawaguchi R, Maruyama T (2002b) Nucleotide specificity of an archaeal group II chaperonin from Thermococcus strain KS-1 with reference to the ATP-dependent protein folding cycle. FEBS Lett 514(2–3):269–274PubMedCrossRefGoogle Scholar
  104. Zako TIR, Okochi M, Nomura T, Ueno T, Tadakuma H, Yohda M, Funatsu T (2005) Facilitated release of substrate protein from prefoldin by chaperonin. FEBS Lett 579(17):3718–3724PubMedCrossRefGoogle Scholar
  105. Zako T, Murase Y, Iizuka R, Yoshida T, Kanzaki T, Ide N, Maeda M, Funatsu T, Yohda M (2006) Localization of prefoldin interaction sites in the hyperthermophilic group II chaperonin and correlations between binding rate and protein transfer rate. J Mol Biol 364(1):110–120PubMedCrossRefGoogle Scholar
  106. Zhang J, Baker ML, Schroder GF, Douglas NR, Reissmann S, Jakana J, Dougherty M, Fu CJ, Levitt M, Ludtke SJ, Frydman J, Chiu W (2010) Mechanism of folding chamber closure in a group II chaperonin. Nature 463(7279):379–383PubMedCrossRefGoogle Scholar
  107. Zwickl P, Grziwa A, Puhler G, Dahlmann B, Lottspeich F, Baumeister W (1992) Primary structure of the Thermoplasma proteasome and its implications for the structure, function, and evolution of the multicatalytic proteinase. Biochemistry 31(4):964–972PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyUniversity of MarylandBaltimoreUSA

Personalised recommendations