Protein folding in vivo revisited

Current Protein and Peptide Science

Volumn 14, Issue 8, 2013, Pages 721-733

  Choi, Seong Il ^a   Kwon, Soonbin ^a   Son, Ahyun ^a   Jeong, Hotcherl ^b   Kim, Kyun Hwan ^c   Seong, Baik L ^a  

^a Yonsei University   (South Korea)

^b Vismer Co Ltd   (South Korea)

^c Konkuk University   (South Korea)

Author keywords

Aggregation; Anfinsen postulate; Excluded volume; Macromolecules; Molecular chaperones; Protein folding; Surface charges

Indexed keywords

CHAPERONE; CHAPERONIN 60; CIS ACTING ELEMENT; EARLY PREGNANCY FACTOR; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR; PROTEIN DNAK; RNA BINDING PROTEIN;

ALLELE; BIOGENESIS; GAIN OF FUNCTION MUTATION; IMMUNOPRECIPITATION; LOSS OF FUNCTION MUTATION; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN PROCESSING; REVIEW; RNA INTERFERENCE; THERMODYNAMICS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ANIMALS; HUMANS; MACROMOLECULAR SUBSTANCES; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 84891792319     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920371408131227170544     Document Type: Review

References (135)

1. Hemmingsen, S.M.; Woolford, C.; van der Vies, S.M.; Tilly, K.; Dennis, D.T.; Georgopoulos, C.P.; Hendrix, R.W.; Ellis, R.J. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature, 1988, 333, 330-334.
2. Gething, M.J.; Sambrook, J. Protein folding in the cell. Nature, 1992, 355, 33-45.
3. Bukau, B.; Horwich, A.L. The Hsp70 and Hsp60 chaperone machines. Cell, 1998, 92, 351-366.
4. Hartl, F.U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 2002, 295, 1852-1858.
5. Anfinsen, C.B. Principles that govern the folding of protein chains. Science, 1973, 181, 223-230.
6. Cheng, M.Y.; Hartl, F.U.; Martin, J.; Pollock, R.A.; Kalousek, F.; Neupert, W.; Hallberg, E.M.; Hallberg, R.L.; Horwich, A.L. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature, 1989, 337, 620-625.
7. Horwich, A.L.; Low, K.B.; Fenton, W.A.; Hirshfield, I.N.; Furtak, K. Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell, 1993, 74, 909-917.
8. Hartl, F.U.; Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol., 2009, 16, 574-581.
9. Choi, S.I.; Ryu, K.; Seong, B.L. RNA-mediated chaperone type for de novo protein folding. RNA Biol., 2009, 6, 21-24.
10. Choi, S.I.; Lim, K.H.; Seong, B.L. Chaperoning roles of macromolecules interacting with proteins in vivo. Int. J. Mol. Sci., 2011, 12, 1979-1990.
11. Choi, S.I.; Son, A.; Lim, K.H.; Jeong, H.; Seong, B.L. Macromolecule-Assisted de novo Protein Folding. Int. J. Mol. Sci., 2012, 13, 10368-10386.
12. Masters, M.; Blakely, G.; Coulson, A.; McLennan, N.; Yerko, V.; Acord, J. Protein folding in Escherichia coli: the chaperonin GroE and its substrates. Res. Microbiol., 2009, 160, 267-277.
13. Kim, C.W.; Han, K.S.; Ryu, K.S.; Kim, B.H.; Kim, K.H.; Choi, S.I.; Seong, B.L. N-terminal domains of native multidomain proteins have the potential to assist de novo folding of their downstream domains in vivo by acting as solubility enhancers. Protein Sci., 2007, 16, 635-643.
14. Sørensen, H.P.; Kristensen, J.E.; Sperling-Petersen, H.U.; Mortensen, K.K. Soluble expression of aggregating proteins by covalent coupling to the ribosome. Biochem. Biophys. Res. Commun., 2004, 319, 715-719.
15. Schimmele, B.; Gräfe, N.; Plückthun, A. Ribosome display of mammalian receptor domains. Protein Eng. Des. Sel., 2005, 18, 285-294.
16. Wittrup, K.D. Protein engineering by cell-surface display. Curr. Opin. Biotechnol., 2001, 12, 395-399.
17. Ngo, K.X.; Umakoshi, H.; Shimanouchi, T.; Sugaya, H.; Kuboi, R. Chitosanase displayed on liposome can increase its activity and stability. J. Bacteriol., 2010, 146, 105-113.
18. Ryu, K.; Kim, C.W.; Kim, B.H.; Han, K.S.; Kim, K.H.; Choi, S.I.; Seong, B.L. Assessment of substrate-stabilizing factors for DnaK on the folding of aggregation-prone proteins. Biochem. Biophys. Res. Commun., 2008, 373, 74-79.
19. Tompa, P.; Csermely, P. The role of structural disorder in the function of RNA and protein chaperones. FASEB J., 2004, 18, 1169-1175.
20. Santner, A.A.; Croy, C.H.; Vasanwala, F.H.; Uversky, V.N.; Van, Y.Y.; Dunker, A.K. Sweeping away protein aggregation with entropic bristles: intrinsically disordered protein fusions enhance soluble expression. Biochemistry, 2012, 51, 7250-7262.
21. Wayne, N.; Bolon, D.N. Charge-rich regions modulate the antiaggregation activity of Hsp90. J. Mol. Biol., 2010, 401, 931-939.
22. De Los Rios, P.; Ben-Zvi, A.; Slutsky, O.; Azem, A.; Goloubinoff, P. Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling. Proc. Natl. Acad. Sci. USA., 2006, 103, 6166-6171.
23. Yang, W.Y.; Gruebele, M. Folding at the speed limit. Nature, 2003, 423, 193-197.
24. Creighton, T.E. In: Protein folding; Garel, G.E., Ed.; W.H. Freeman and Company: New York, 1992; pp. 405-454.
25. Netzer, W.J.; Hartl, F.U. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature, 1997, 388, 343-349.
26. Inaba, K.; Kobayashi, N.; Fersht, A.R. Conversion of two-state to multi-state folding kinetics on fusion of two protein foldons. J. Mol. Biol., 2000, 302, 219-233.
27. Kolb, V.A.; Makeyev, E.V.; Spirin, A.S. Folding of firefly luciferase during translation in a cell-free system. EMBO J., 1994, 13, 3631-3637.
28. Fedorov, A.N.; Baldwin, T.O. Cotranslational protein folding. J. Biol. Chem., 1997, 272, 32715-32718.
29. Kramer, G.; Ramachandiran, V.; Hardesty, B. Cotranslational folding-omnia mea mecum porto? Int. J. Biochem. Cell. Biol., 2001, 33, 541-553.
30. Frydman, J.; Erdjument-Bromage, H.; Tempst, P.; and Hartl, F.U. Co-translational domain folding as the structural basis for the rapid de novo folding of firefly luciferase. Nat. Struct. Biol., 1999, 6, 697-705.
31. Uversky, V.N.; Fink, A.L. In: Protein Misfolding, Aggregation, and Conformational Diseases; Uversky, V.N.; Fernández, A.; Fink, A.L., Eds.; Springer Science+Business Media: New York, 2006, Vol. 4, pp. 1-20.
32. Shaw, K.L.; Grimsley, G.R.; Yakovlev, G.I.; Makarov, A. A; Pace, C.N. The effect of net charge on the solubility, activity, and stability of ribonuclease Sa. Protein Sci., 2001, 10, 1206-1215.
33. Chiti, F.; Stefani, M.; Taddei, N.; Ramponi, G.; Dobson, C.M. Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature, 2003, 424, 805-808.
34. Lawrence, M.S.; Phillips, K.J.; Liu, D.R. Supercharging proteins can impart unusual resilience. J. Am. Chem. Soc., 2007, 129, 10110-10112.
35. Hua, Q.X.; Jia, W.; Frank, B.H.; Phillips, N.F.; Weiss, M.A. A protein caught in a kinetic trap: structures and stabilities of insulin disulfide isomers. Biochemistry, 2002, 41, 14700-14715.
36. Sohl, J.L.; Jaswal, S.S.; Agard, D.A. Unfolded conformations of α-lytic protease are more stable than its native state. Nature, 1998, 395, 817-819.
37. Wang, Z.; Mottonen, J.; Goldsmith, E.J. Kinetically controlled folding of the serpin plasminogen activator inhibitor 1. Biochemistry, 1996, 35, 16443-16448.
38. Dunker, A.K.; Silman, I.; Uversky, V.N.; Sussman, J.L. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol., 2008, 18, 756-764.
39. Xue, B.; Williams, R.W.; Oldfield, C.J.; Dunker, A.K.; Uversky, V.N. Archaic chaos: Intrinsically disordered proteins in Archaea. BMC Syst. Biol., 2010, 4, S1.
40. Uversky, V.N.; Gillespie, J.R.; Fink, A.L. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins, 2000, 41, 415-427.
41. Babu, M.M.; van der Lee, R.; de Groot, N.S.; Gsponer, J. Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol., 2011, 21, 432-440.
42. Bolen, D.W.; Rose, G.D. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem., 2008, 77, 339-362.
43. Dill, K.A.; Ozkan, S.B.; Shell, M.S.; Weikl T.R. The protein folding problem. Annu Rev Biophys., 2008, 37, 289-316.
44. Agashe, V.R.; Guha, S.; Chang, H.C.; Genevaux, P.; Hayer-Hartl, M.; Stemp, M.; Georgopoulos, C.; Hartl, F.U.; Barral, J.M.; Function of trigger factor and DnaK in multidomain protein folding: increase in yield at the expense of folding speed. Cell, 2004, 117, 199-209.
45. Brinker, A.; Pfeifer, G.; Kerner, M.J.; Naylor, D.J.; Hartl, F.U.; Hayer-Hartl, M. Dual function of protein confinement in chaperonin-assisted protein folding. Cell, 2001, 107, 223-233.
46. Tang, Y.C.; Chang, H.C.; Roeben, A.; Wischnewski, D.; Wischnewski, N.; Kerner, M.J.; Hartl, F.U.; Hayer-Hartl, M. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell, 2006, 125, 903-914.
47. Chakraborty, K.; Chatila, M.; Sinha, J.; Shi, Q.; Poschner, B.C.; Sikor, M.; Jiang, G.; Lamb, D.C.; Hartl, F.U.; Hayer-Hartl, M. Chaperonin-catalyzed rescue of kinetically trapped states in protein folding. Cell, 2010, 142, 112-122.
48. Apetri, A.C.; Horwich, A.L. Chaperonin chamber accelerates protein folding through passive action of preventing aggregation. Proc. Natl. Acad. Sci. USA., 2008, 105, 17351-17355.
49. Tyagi, N.K.; Fenton, W.A.; Deniz, A.A.; Horwich, A.L. Double mutant MBP refolds at same rate in free solution as inside the GroEL/GroES chaperonin chamber when aggregation in free solution is prevented. FEBS Lett., 2011, 585, 1969-1972.
50. Gruebele, M. Downhill protein folding: evolution meets physics. C.R. Biol., 2005, 328, 701-712.
51. Deuerling, E.; Schulze-Specking, A.; Tomoyasu, T.; Mogk, A.; Bukau, B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature, 1999, 400, 693-696.
52. Vorderwülbecke, S.; Kramer, G.; Merz, F.; Kurz, T.A.; Rauch, T.; Zachmann-Brand, B.; Bukau, B.; Deuerling, E. Low temperature of GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. FEBS Lett., 2004, 559, 181-187.
53. Ullers, R.S.; Luirink, J.; Harms, N.; Schwager, F.; Georgopoulos, C.; Genevaux, P. SecB is a bona fide generalized chaperone in Escherichia coli. Proc. Natl. Acad. Sci. USA., 2004, 101, 7583-7588.
54. Bruel, N.; Castanie-Cornet, M.P.; Cirinesi, A.M.; Koningstein, G.; Georgopoulos, C.; Luirink, J.; Genevaux, P.; Hsp33 controls Elongation Factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and Trigger Factor chaperones. J. Biol. Chem., 2012, 287, 44435-44446.
55. Kandror, O., Busconi, L, Sherman, M., Goldberg, A.L. Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES. J. Biol. Chem. 1994, 269, 23575-23582.
56. Kandror, O., Sherman, M., Rhode, M., Goldberg, A.L. Trigger factor is involved in GroEL-dependent protein degradation in Escherichia coli and promotes binding of GroEL to unfolded proteins. EMBO J., 1995, 14, 6021-6027.
57. 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.
58. Chapman, E.; Farr, G.W.; Usaite, R.; Furtak, K.; Fenton, W.A.; Chaudhuri, T.K.; Hondorp, E.R.; Matthews, R.G.; Wolf, S.G.; Yates, J.R.; Pypaert, M., Horwich, A.L. Global aggregation of newly translated proteins in an Escherichia coli strain deficient of the chaperonin GroEL. Proc. Natl. Acad. Sci. USA., 2006, 103, 15800-15805.
59. Sewell, B.T.; Best, R.B.; Chen, S.; Roseman, A.M.; Farr, G.W.; Horwich, A.L.; Saibil, H.R. A mutant chaperonin with rearranged inter-ring electrostatic contacts and temperature-sensitive dissociation. Nat. Struct. Mol. Biol., 2004, 11, 1128-1133.
60. Sot, B.; von Germar, F.; Mäntele, W.; Valpuesta, J.M.; Taneva, S.G.; Muga, A. Ionic interactions at both inter-ring contact sites of GroEL are involved in transmission of the allosteric signal: a timeresolved infrared difference study. Protein Sci., 2005, 14, 2267-2274.
61. Bross, P.; Naundrup, S.; Hansen, J.; Nielsen, M.N.; Christensen, J.H.; Kruhøffer, M.; Palmfeldt, J.; Corydon, T.J.; Gregersen, N.; Ang, D.; Georgopoulos, C.; Nielsen, K.L. The Hsp60-(p. V98I) mutation associated with hereditary spastic paraplegia SPG13 compromises chaperonin function both in vitro and in vivo. J. Biol. Chem., 2008, 283, 15694-15700.
62. Georgopoulos, C.P.; Hendrix, R.W.; Casjens, S.R.; Kaiser, A.D. Host participation in bacteriophage lambda head assembly. J. Mol. Biol., 1973, 76, 45-60.
63. Sternberg, N. Properties of a mutant of Escherichia coli defective in bacteriophage lambda head formation (groE). II. The propagation of phage lambda. J. Mol. Biol., 1973, 76, 25-44.
64. Takano, T.; Kakefunda, T. Involvement of a bacterial factor in morphogenesis of bacteriophage capsid. Nature New Biol., 1972, 239, 34-37.
65. Ang, D.; Keppel, F.; Klein G.; Richardson, A.; Georgopoulos, C. Genetic analysis of bacteriophage-encoded cochaperonins. Annu. Rev. Genet., 2000, 34, 439-456.
66. Houry, W.A.; Frishman, D.; Eckerskorn, C.; Lottspeich, F.; Hartl, F.U. Identification of in vivo substrates of the chaperonin GroEL. Nature, 1999, 402, 147-154.
67. Kerner, M.J.; Naylor, D.J.; Ishihama, Y.; Maier, T.; Chang, H.C.; Stines, A.P.; Georgopoulos, C.; Frishman, D.; Hayer-Hartl, M.; Mann, M.; Hartl, F.U. Proteome-wide analysis of chaperonindependent protein folding in Escherichia coli. Cell, 2005, 122, 209-220.
68. Fujiwara, K.; Ishihama, Y.; Nakahigashi, K.; Soga, T.; Taguchi, H. A systematic survey of in vivo obligate chaperonin-dependent substrates. EMBO J., 2010, 29, 1552-1564.
69. Koll, H.; Guiard, B.; Rassow, J.; Ostermann, J.; Horwich, A.L.; Neupert, W.; Hartl, F.U. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell, 1992, 68, 1163-1175.
70. Cabrita, L.D.; Dobson, C.M.; Christodoulou, J. Protein folding on the ribosome. Curr. Opin. Struct. Biol., 2010, 20, 33-45.
71. Eichmann, C.; Preissler, S.; Riek, R.; Deuerling, E. Cotranslational structure acquisition of nascent polypeptides monitored by NMR spectroscopy. Proc. Natl. Acad. Sci. USA., 2010, 107, 9111-9116.
72. Uversky, V.N.; Dunker, A.K. Understanding protein non-folding. Biochim. Biophys. Acta., 2010, 1804, 1231-1264.
73. Dyson, H.J.; Wright, P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell. Biol., 2005, 6, 197-208.
74. Fernández, A.; Crespo, A. Protein wrapping: a molecular marker for association, aggregation and drug design. Chem. Soc. Rev., 2008, 37, 2373-2382.
75. Li, C.; Schwabe, J.W.; Banayo, E.; Evans, R.M. Coexpression of nuclear receptor partners increases their solubility and biological activities. Proc. Natl. Acad. Sci. USA., 1997, 94, 2278-2283.
76. Fribourg, S.; Romier, C.; Werten, S.; Gangloff, Y.G.; Poterszman, A.; Moras, D. Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli. J. Mol. Biol., 2001, 306, 363-373.
77. Mossakowska, D.E. Expression of nuclear hormone receptors in Escherichia coli. Curr. Opin. Biotechnol., 1998, 9, 502-505.
78. Hartl, F.U.; Bracher, A.; Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature, 2011, 475, 324-332.
79. Powers, E.T.; Morimoto, R.I.; Dillin, A.; Kelly, J.W.; Balch, W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem., 2009, 78, 959-991.
80. Wang, C.C.; Schimmel, P. Species barrier to RNA recognition overcome with nonspecific RNA binding domains. J. Biol. Chem., 1999, 274, 16508-16512.
81. Henics, T. Extending the 'stressy' edge: molecular chaperones flirting with RNA. Cell Biol. Int., 2003, 27, 1-6.
82. Ellis, R.J. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol., 2001, 11, 114-119.
83. Draper, D.E. Themes in RNA-protein recognition. J. Mol. Biol., 1999, 293, 255-270.
84. Lund, B.M.; Moore, C.; Varami, G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol., 2007, 8, 479-490.
85. Chattopadhyay, S.; Das, B.; Dasgupta, C. Reactivation of denatured proteins by 23S ribosomal RNA: role of domain V. Proc. Natl. Acad. Sci. USA., 1996, 93, 8284-8287.
86. Sulijoadikusumo, I.; Horikoshi, N.; Usheva, A. Another function for the mitochondrial ribosomal RNA: protein folding. Biochemistry, 2001, 40, 11559-11564.
87. Choi, S.I.; Han, K.S.; Kim, C.W.; Ryu, K.S.; Kim, B.H.; Kim, K.H.; Kim, S.I.; Kang, T.H.; Shin, H.C.; Lim, K.H.; Kim, H.K.; Hyun, J.M.; Seong, B.L. Protein solubility and folding enhancement by interaction with RNA. PLoS ONE, 2008, 3, e2677.
88. Kim, H.K.; Choi, S.I.; Seong, B.L. 5S rRNA-assisted DnaK refolding. Biochem. Biophys. Res. Commun., 2010, 391, 1177-1181.
89. Ghosh, J.; Basu, A.; Pal, S.; Chowdhuri, S.; Bhattacharya, A.; Pal, D.; Chattoraj, D.K.; DasGupta, C. Ribosome-DnaK interactions in relation to protein folding. Mol. Microbiol., 2003, 48, 1679-1692.
90. Rentzeperis, D.; Jonsson, T.; Sauer, R.T. Acceleration of the refolding of Arc repressor by nucleic acids and other polyanions. Nat. Struct. Biol., 1999, 6, 569-573.
91. King, O.D.; Gitler, A.D.; Shorter, J. The tip of the iceberg: RNAbinding proteins with prion-like domains in neurodegenerative disease. Brain Res., 2012, 1462, 61-80.
92. Deleault, N.R.; Lucassen, R.W.; Supattapone, S. RNA molecules stimulate prion protein conversion. Nature, 2003, 425, 717-720.
93. Ellis, R.J.; Hartl, F.U. Principles of protein folding in the cellular environment. Curr. Opin. Struct. Biol., 1999, 9, 102-110.
94. Feldman, D.E.; Frydman, J. Protein folding in vivo: The importance of molecular chaperones. Curr. Opin. Struct. Biol., 2000, 10, 26-33.
95. Pelham, H.R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell, 1986, 46, 959-961.
96. Wegrzyn, R.D.; Deuerling, E. Molecular guardians for newborn proteins: ribosome-associated chaperones and their role in protein folding. Cell. Mol. Life Sci., 2005, 62, 2727-2738.
97. Peisker, K.; Chiabudini, M.; Rospert, S. The ribosome-bound Hsp70 homolog Ssb of Saccharomyces cerevisiae. Biochim. Biophys. Acta., 2010, 1803, 662-672.
98. Kaiser, C.M.; Goldman, D.H.; Chodera, J.D.; Tinoco, I. Jr; Bustamante, C. The ribosome modulates nascent protein folding. Science, 2011, 334, 1723-1727.
99. Svetlov, M.S.; Kolb, V.A.; Spirin, A.S. Folding of the firefly luciferase polypeptide chain with immobilized C-terminus. Mol. Biol. (Mosk), 2007, 41, 96-102.
100. Fagerberg, L.; Jonasson, K.; von Heijne, G.; Uhlén, M.; Berglund, L. Prediction of the human membrane proteome. Proteomics, 2010, 10, 1141-1149.
101. Jose, J. Autodisplay: efficient bacterial surface display of recombinant proteins. Appl. Microbiol. Biotechnol., 2006, 69, 607-614.
102. Chen, Y.P.; Hwang, I.E.; Lin, C.J.; Wang, H.J.; Tseng C.P. Enhancing the stability of xylanase from Cellulomonas fimi by cell-surface display on Escherichia coli. J. Appl. Microbiol., 2012, 112, 455-463.
103. Braun, P.; LaBaer, J. High throughput protein production for functional proteomics. Trends Biotechnol., 2003, 21, 383-388.
104. Esposito, D.; Chatterjee, D.K. Enhancement of soluble protein expression through the use of fusion tags. Curr. Opin. Biotechnol., 2006, 17, 353-358.
105. Aoki, K.; Taguchi, H.; Shindo, Y.; Yoshida, M.; Ogasahara, K.; Yutani, K.; Tanaka, N. Calorimetric observation of a GroELprotein binding reaction with little contribution of hydrophobic interaction. J. Biol. Chem., 1997, 272, 32158-32162.
106. Misselwitz, B.; Staeck, O.; Rapoport, T.A. J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Mol. Cell, 1998, 2, 593-603.
107. Martinez-Hackert, E.; Hendrickson, W.A. Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell, 2009, 138, 923-934.
108. Trombetta, E.S.; Helenius, A. Lectins as chaperones in glycoprotein folding. Curr. Opin. Struct. Biol., 1998, 8, 587-592.
109. Samanta, D.; Mukhopadhyay, D.; Chowdhury, S.; Ghosh, J.; Pal, S.; Basu, A.; Bhattacharya, A.; Das, A.; Das, D.; DasGupta, C. Protein folding by domain V of Escherichia coli 23S rRNA: specificity of RNA-protein interactions. J. Bacteriol., 2008, 190, 3344-3352.
110. Rüdiger, S.; Germeroth, L.; Schneider-Mergener, J.; Bukau, B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J., 1997, 16, 1501-1507.
111. Basters, A.; Ketscher, L.; Deuerling, E.; Arkona, C.; Rademann, J.; Knobeloch, K.P.; Fritz, G. High yield expression of catalytically active USP18 (UBP43) using a Trigger Factor fusion system. BMC Biotechnol., 2012, 12, 56.
112. Kyratsous, C.A.; Panagiotidis, C.A. Heat-shock protein fusion vectors for improved expression of soluble recombinant proteins in Escherichia coli. Methods Mol. Biol., 2012, 824, 109-129.
113. Otzen, D.E.; Kristensen, O.; Oliveberg, M. Designed protein tetramer zipped together with a hydrophobic Alzheimer homology: a structural clue to amyloid assembly. Proc. Natl. Acad. Sci. USA., 2000, 97, 9907-9912.
114. Chiti, F.; Calamai, M.; Taddei, N.; Stefani, M.; Ramponi, G.; Dobson, C.M. Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc. Natl. Acad. Sci. USA., 2002, 99, 16419-16426.
115. 2 subunit ectodomain. Biochemistry, 1998, 37, 13643-13649.
116. Zhang, Y.B.; Howitt, J.; McCorkle, S.; Lawrence, P.; Springer, K.; Freimuth, P. Protein aggregation during overexpression limited by peptide extensions with large net negative charge. Protein Expr. Purif., 2004, 36, 207-216.
117. Davis, G.D.; Elisee, C.; Newham, D.M.; and Harrison, R.G. New fusion protein systems designed to give soluble expression in Escherichia coli Biotechnol. Bioeng., 1999, 65, 382-388.
118. Tokunaga, H.; Saito, S., Sakai, K.; Yamaguchi, R.; Katsuyama, I.; Arakawa, T.; Onozaki, K.; Arakawa, T.; Tokunaga, M. Halophilic beta-lactamase as a new solubility-and folding-enhancing tag protein: production of native human interleukin 1alpha and human neutrophil alpha-defensin. Appl. Microbiol. Biotechnol., 2010, 86, 649-658.
119. Speed, M.A.; Wang, D.I.; King, J. Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat. Biotechnol., 1996, 14, 1283-1287.
120. Rajan, R.S.; Illing, M.E.; Bence, N.F.; Kopito, R.R. Specificity in intracellular protein aggregation and inclusion body formation. Proc. Natl. Acad. Sci. USA., 2001, 98, 13060-13065.
121. Wright, C.F.; Teichmann, S.A.; Clarke, J.; Dobson, C.M. The importance of sequence diversity in the aggregation and evolution of proteins. Nature, 2005, 438, 878-881.
122. Fink, A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des., 1998, 3, R9-R23.
123. Høiberg-Nielsen, R.; Fuglsang, C.C.; Arleth, L.; Westh, P. Interrelationships of glycosylation and aggregation kinetics for Peniophora lycii phytase. Biochemistry, 2006, 45, 5057-5066.
124. Rajan, R.S.; Li, T.; Aras, M.; Sloey, C.; Sutherland, W.; Arai, H.; Briddell, R.; Kinstler, O.; Lueras, A.M.; Zhang, Y.; Yeghnazar, H.; Treuheit, M.; Brems, D.N. Modulation of protein aggregation by polyethylene glycol conjugation: GCSF as a case study. Protein Sci., 2006, 15, 1063-1075.
125. rd ed.; Taylor & Francis: 1997, pp. 575-621.
126. 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, 2001, 107, 235-246.
127. Wang, Q.; Buckle, A.M.; Foster, N.W.; Johnson, C.M.; Fersht, A.R. Design of highly stable functional GroEL minichaperones. Protein Sci., 1999, 8, 2186-2193.
128. Ban, N.; Nissen, P.; Hansen, J.; Moore, P.B.; Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2. 4 Å resolution. Science, 2000, 289, 905-920.
129. Panavas, T.; Sanders, C.; Butt, T.R. SUMO fusion technology for enhanced protein production in prokaryotic and eukaryotic expression systems. Methods Mol. Biol., 2009, 497, 303-317.
130. Baker, R.T. Protein expression using ubiquitin fusion and cleavage. Curr. Opin. Biotechnol., 1996, 7, 541-546.
131. Muchowski, P.J.; Wacker, J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci., 2005, 6, 11-22.
132. Zhou, H.X.; Rivas, G.; Minton, A.P. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu. Rev. Biophys., 2008, 37, 375-397.
133. van den Berg, B.; Ellis, R.J.; Dobson, C.M. Effects of macromolecular crowding on protein folding and aggregation. EMBO J., 1999, 18, 6927-6933.
134. Zimmerman, S.B.; Harrison, B. Macromolecular crowding increases binding of DNA polymerase to DNA: an adaptive effect. Proc. Natl. Acad. Sci. USA., 1987, 84, 1871-1875.
135. Seeliger, J.; Werkmüller, A.; Winter, R. Macromolecular crowding as a suppressor of human IAPP fibril formation and cytotoxicity. PLoS One, 2013, 8, e69652.