Converging concepts of protein folding in vitro and in vivo

Nature Structural and Molecular Biology

Volumn 16, Issue 6, 2009, Pages 574-581

  Hartl, F Ulrich ^a   Hayer Hartl, Manajit ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; AMYLOID; BACTERIAL PROTEIN; CHAPERONE; CHAPERONIN; CONNECTIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; OLIGOMER; PROTEIN DNAJ; PROTEIN DNAK; TRIGGER FACTOR; UNCLASSIFIED DRUG;

AGING; ALPHA HELIX; ALZHEIMER DISEASE; ARCHAEBACTERIUM; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HUMAN; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; GROEL PROTEIN; GROES PROTEIN; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN FOLDING; PROTEINS;

EID: 66849143696     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1591     Document Type: Review

References (104)

1. Anfinsen, C.B. Principles that govern the folding of protein chains. Science 181, 223-230 (1973).
2. Hartl, F.U. Molecular chaperones in cellular protein folding. Nature 381, 571-579 (1996).
3. Bartlett, A.L. & Radford, S.E. An expanding arsenal of experimental methods yields an explosion of insights into protein folding mechanisms. Nat. Struct. Mol. Biol. 16, 582-588 (2009).
4. Brockwell, D.J. & Radford, S.E. Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17, 30-37 (2007).
5. Onuchic, J.N. & Wolynes, P.G. Theory of protein folding. Curr. Opin. Struct. Biol. 14, 70-75 (2004).
6. Jahn, T.R. & Radford, S.E. The Yin and Yang of protein folding. FEBS J. 272, 5962-5970 (2005).
7. Englander, S.W., Mayne, L. & Krishna, M.M. Protein folding and misfolding: mechanism and principles. Q. Rev. Biophys. 40, 287-326 (2007).
8. Lindberg, M.O. & Oliveberg, M. Malleability of protein folding pathways: a simple reason for complex behaviour. Curr. Opin. Struct. Biol. 17, 21-29 (2007).
9. Netzer, W.J. & Hartl, F.U. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature 388, 343-349 (1997).
10. Wright, C.F., Teichmann, S.A., Clarke, J. & Dobson, C.M. The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438, 878-881 (2005).
11. Dobson, C.M. Protein folding and misfolding. Nature 426, 884-890 (2003).
12. Ignatova, Z. & Gierasch, L.M. Monitoring protein stability and aggregation in vivo by real-time fluorescent labeling. Proc. Natl. Acad. Sci. USA 101, 523-528 (2004).
13. Ellis, R.J. & Minton, A.P. Protein aggregation in crowded environments. Biol. Chem. 387, 485-497 (2006).
14. Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution. Science 289, 905-920 (2000).
15. Lu, J.L. & Deutsch, C. Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 12, 1123-1129 (2005).
16. Woolhead, C.A., McCormick, P.J. & Johnson, A.E. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116, 725-736 (2004).
17. Kramer, G., Boehringer, D., Ban, N. & Bukau, B. The ribosome as a platform for cotranslational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597 (2009).
18. Elcock, A.H. Molecular simulations of cotranslational protein folding: fragment stabilities, folding cooperativity, and trapping in the ribosome. PLOS Comput. Biol. 2, e98 (2006).
19. Kaiser, C.M. et al. Real-time observation of trigger factor function on translating ribosomes. Nature 444, 455-460 (2006).
20. Vabulas, R.M. & Hartl, F.U. Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310, 1960-1963 (2005).
21. Maisnier-Patin, S. et al. Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nat. Genet. 37, 1376-1379 (2005).
22. Tang, Y.C. et al. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 125, 903-914 (2006).
23. Rutherford, S.L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342 (1998).
24. Kerner, M.J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
25. Chang, H.C., Tang, Y.C., Hayer-Hartl, M. & Hartl, F.U. SnapShot: molecular chaper-ones, Part I. Cell 128, 212 (2007).
26. Tang, Y.C., Chang, H.C., Hayer-Hartl, M. & Hartl, F.U. SnapShot: molecular chaper-ones, Part II. Cell 128, 412 (2007).
27. Weibezahn, J., Schlieker, C., Tessarz, P., Mogk, A. & Bukau, B. Novel insights into the mechanism of chaperone-assisted protein disaggregation. Biol. Chem. 386, 739-744 (2005).
28. Balch, W.E., Morimoto, R.I., Dillin, A. & Kelly, J.W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008).
29. Frydman, J. Folding of newly translated proteins in vivo: The role of molecular chaperones. Annu. Rev. Biochem. 70, 603-647 (2001).
30. Hartl, F.U. & Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858 (2002).
31. Langer, T. et al. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356, 683-689 (1992).
32. Albanèse, V., Yam, A.Y.W., Baughman, J., Parnot, C. & Frydman, J. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 124, 75-88 (2006).
33. Otto, H. et al. The chaperones MPP11 and Hsp70L1 form the mammalian ribosome-associated complex. Proc. Natl. Acad. Sci. USA 102, 10064-10069 (2005).
34. Hundley, H.A., Walter, W., Bairstow, S. & Craig, E.A. Human Mpp11 J protein: ribosome-tethered molecular chaperones are ubiquitous. Science 308, 1032-1034 (2005).
35. Brandt, F. et al. The native 3D organization of bacterial polysomes. Cell 136, 261-271 (2009).
36. Agashe, V.R. et al. Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell 117, 199-209 (2004).
37. Frydman, J., Nimmesgern, E., Ohtsuka, K. & Hartl, F.U. Folding of nascent polypep-tide chains in a high molecular mass assembly with molecular chaperones. Nature 370, 111-117 (1994).
38. Wandinger, S.K., Richter, K. & Buchner, J. The Hsp90 chaperone machinery. J. Biol. Chem. 283, 18473-18477 (2008).
39. Cuéllar, J. et al. The structure of CCT-Hsc70 NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin. Nat. Struct. Mol. Biol. 15, 858-864 (2008).
40. Vainberg, I.E. et al. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93, 863-873 (1998).
41. McCallum, C.D., Do, H., Johnson, A.E. & Frydman, J. The interaction of the chaperonin tailless complex polypeptide 1 (TCP1) ring complex (TRiC) with ribo-some-bound nascent chains examined using photo-cross-linking. J. Cell Biol. 149, 591-602 (2000).
42. Thulasiraman, V., Yang, C.F. & Frydman, J. In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 18, 85-95 (1999).
43. Siegers, K. et al. Compartmentation of protein folding in vivo: sequestration of non-native polypeptide by the chaperonin-GimC system. EMBO J. 18, 75-84 (1999).
44. Zhao, R. & Houry, W.A. Molecular interaction network of the Hsp90 chaperone system. Adv. Exp. Med. Biol. 594, 27-36 (2007).
45. Ellis, R.J. Molecular chaperones: assisting assembly in addition to folding. Trends Biochem. Sci. 31, 395-401 (2006).
46. Saschenbrecker, S. et al. Structure and function of RbcX, an assembly chaperone for hexadecameric rubisco. Cell 129, 1189-1200 (2007).
47. Teter, S.A. et al. Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97, 755-765 (1999).
48. Deuerling, E., Schulze-Specking, A., Tomoyasu, T., Mogk, A. & Bukau, B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400, 693-696 (1999).
49. Ewalt, K.L., Hendrick, J.P., Houry, W.A. & Hartl, F.U. In vivo observation of polypep-tide flux through the bacterial chaperonin system. Cell 90, 491-500 (1997).
50. Dekker, C. et al. The interaction network of the chaperonin CCT. EMBO J 27, 1827-1839 (2008).
51. Yam, A.Y. et al. Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat. Struct. Mol. Biol. 15, 1255-1262 (2008).
52. Kleizen, B. & Braakman, I. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16, 343-349 (2004).
53. Skach, W.R. Cellular mechanisms of membrane protein folding. Nat. Struct. Mol. Biol. 16, 606-612 (2009).
54. Ferbitz, L. et al. Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431, 590-596 (2004).
55. Lakshmipathy, S.K. et al. Identification of nascent chain interaction sites on Trigger factor. J. Biol. Chem. 282, 12186-12193 (2007).
56. Merz, F. et al. Molecular mechanism and structure of Trigger factor bound to the translating ribosome. EMBO J. 27, 1622-1632 (2008).
57. Merz, F. et al. The C-terminal domain of Escherichia coli Trigger factor represents the central module of its chaperone activity. J. Biol. Chem. 281, 31963-31971 (2006).
58. Schlünzen, F. et al. The binding mode of the Trigger factor on the ribosome: implications for protein folding and SRP interaction. Structure 13, 1685-1694 (2005).
59. Baram, D. et al. Structure of Trigger factor binding domain in biologically homologous complex with eubacterial ribosome reveals its chaperone action. Proc. Natl. Acad. Sci. USA 102, 12017-12022 (2005).
60. Mayer, M.P., Rudiger, S. & Bukau, B. Molecular basis for interactions of the DnaK chaperone with substrates. Biol. Chem. 381, 877-885 (2000).
61. Zhu, X. et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272, 1606-1614 (1996).
62. Rüdiger, S., Buchberger, A. & Bukau, B. Interaction of Hsp70 chaperones with substrates. Nat. Struct. Biol. 4, 342-349 (1997).
63. Pellecchia, M. et al. Structural insights into substrate binding by the molecular chaperone DnaK. Nat. Struct. Biol. 7, 298-303 (2000).
64. Young, J.C., Barral, J.M. & Hartl, F.U. More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28, 541-547 (2003).
65. Schiene-Fischer, C., Habazettl, J., Schmid, F.X. & Fischer, G. The Hsp70 chaperone DnaK is a secondary amide peptide bond cis-trans isomerase. Nat. Struct. Biol. 9, 419-424 (2002).
66. Dragovic, Z., Broadley, S.A., Shomura, Y., Bracher, A. & Hartl, F.U. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 25, 2519-2528 (2006).
67. Raviol, H., Sadlish, H., Rodriguez, F., Mayer, M.P. & Bukau, B. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J. 25, 2510-2518 (2006).
68. Liu, Q. & Hendrickson, W.A. Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131, 106-120 (2007).
69. Polier, S., Dragovic, Z., Hartl, F.U. & Bracher, A. Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133, 1068-1079 (2008).
70. Schuermann, J.P. et al. Structure of the Hsp110: Hsc70 nucleotide exchange machine. Mol. Cell 31, 232-243 (2008).
71. Horwich, A.L., Fenton, W.A., Chapman, E. & Farr, G.W. Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 23, 115-145 (2007).
72. Gromiha, M.M. & Selvaraj, S. Inter-residue interactions in protein folding and stability. Prog. Biophys. Mol. Biol. 86, 235-277 (2004).
73. Xu, Z., Horwich, A.L. & Sigler, P.B. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388, 741-750 (1997).
74. Horst, R. et al. Direct NMR observation of a substrate protein bound to the chaperonin GroEL. Proc. Natl. Acad. Sci. USA 102, 12748-12753 (2005).
75. Sharma, S. et al. Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 133, 142-153 (2008).
76. Hillger, F. et al. Probing protein-chaperone interactions with single-molecule fluorescence spectroscopy. Angew. Chem. Int. Ed. 47, 6184-6188 (2008).
77. Elad, N. et al. Topologies of a substrate protein bound to the chaperonin GroEL. Mol. Cell 26, 415-426 (2007).
78. Brinker, A. et al. Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107, 223-233 (2001).
79. Chaudhuri, T.K., Farr, G.W., Fenton, W.A., Rospert, S. & Horwich, A.L. GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 107, 235-246 (2001).
80. Clare, D.K., Bakkes, P.J., van Heerikhuizen, H., van der Vies, S.M. & Saibil, H.R. Chaperonin complex with a newly folded protein encapsulated in the folding chamber. Nature 457, 107-110 (2009).
81. Apetri, A.C. & Horwich, A.L. Chaperonin chamber accelerates protein folding through passive action of preventing aggregation. Proc. Natl. Acad. Sci. USA 105, 17351-17355 (2008).
82. Lin, Z. & Rye, H.S. Expansion and compression of a protein folding intermediate by GroEL. Mol. Cell 16, 23-34 (2004).
83. Baumketner, A., Jewett, A. & Shea, J.E. Effects of confinement in chaperonin assisted protein folding: rate enhancement by decreasing the roughness of the folding energy landscape. J. Mol. Biol. 332, 701-713 (2003).
84. Hayer-Hartl, M. & Minton, A.P. A simple semiempirical model for the effect of molecular confinement upon the rate of protein folding. Biochemistry 45, 13356-13360 (2006).
85. Tang, Y.C., Chang, H.C., Chakraborty, K., Hartl, F.U. & Hayer-Hartl, M. Essential role of the chaperonin folding compartment in vivo. EMBO J. 27, 1458-1468 (2008).
86. Wang, J.D., Herman, C., Tipton, K.A., Gross, C.A. & Weissman, J.S. Directed evolution of substrate-optimized GroEL/S chaperonins. Cell 111, 1027-1039 (2002).
87. England, J.L., Lucent, D. & Pande, V.S. A role for confined water in chaperonin function. J. Am. Chem. Soc. 130, 11838-11839 (2008).
88. Horst, R., Fenton, W.A., Englander, S.W., Wuthrich, K. & Horwich, A.L. Folding trajectories of human dihydrofolate reductase inside the GroEL GroES chaperonin cavity and free in solution. Proc. Natl. Acad. Sci. USA 104, 20788-20792 (2007).
89. Thirumalai, D. & Lorimer, G.H. Chaperonin-mediated protein folding. Annu. Rev. Biophys. Biomol. Struct. 30, 245-269 (2001).
90. Lin, Z., Madan, D. & Rye, H.S. GroEL stimulates protein folding through forced unfolding. Nat. Struct. Mol. Biol. 15, 303-311 (2008).
91. Koike-Takeshita, A., Yoshida, M. & Taguchi, H. Revisiting the GroEL-GroES reaction cycle via the symmetric intermediate implied by novel aspects of the GroEL(D398A) mutant. J. Biol. Chem. 283, 23774-23781 (2008).
92. Tessier, P. & Lindquist, S. Unraveling molecular interactions and structures of self-perpetuating prions. Nat. Struct. Mol. Biol. 16, 598-605 (2009).
93. Chiti, F. & Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006).
94. Barral, J.M., Broadley, S.A., Schaffar, G. & Hartl, F.U. Roles of molecular chaperones in protein misfolding diseases. Semin. Cell Dev. Biol. 15, 17-29 (2004).
95. Muchowski, P.J. et al. Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. USA 97, 7841-7846 (2000).
96. Muchowski, P.J. & Wacker, J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6, 11-22 (2005).
97. Auluck, P.K., Chan, H.Y.E., Trojanowski, J.Q., Lee, V.M.Y. & Bonini, N.M. Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295, 865-868 (2002).
98. Behrends, C. et al. Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol. Cell 23, 887-897 (2006).
99. Tam, S., Geller, R., Spiess, C. & Frydman, J. The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat. Cell Biol. 8, 1155-1162 (2006).
100. Kitamura, A. et al. Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state. Nat. Cell Biol. 8, 1163-1170 (2006).
101. Morley, J.F. & Morimoto, R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 15, 657-664 (2004).
102. Sittler, A. et al. Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum. Mol. Genet. 10, 1307-1315 (2001).
103. Scheufler, C. et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210 (2000).
104. Harrison, C.J., Hayer-Hartl, M., Di Liberto, M., Hartl, F.U. & Kuriyan, J. Crystal structure of the nucleotide exchange factor GrpE to the ATPase domain of the molecular chaperone DnaK. Science 276, 431-435 (1997).