A Simple Principle for Understanding the Combined Cellular Protein Folding and Aggregation

Author(s): Seong Il Choi*.

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 1 , 2020

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Graphical Abstract:


Abstract:

Proteins can undergo kinetic/thermodynamic partitioning between folding and aggregation. Proper protein folding and thermodynamic stability are crucial for aggregation inhibition. Thus, proteinfolding principles have been widely believed to consistently underlie aggregation as a consequence of conformational change. However, this prevailing view appears to be challenged by the ubiquitous phenomena that the intrinsic and extrinsic factors including cellular macromolecules can prevent aggregation, independently of (even with sacrificing) protein folding rate and stability. This conundrum can be definitely resolved by ‘a simple principle’ based on a rigorous distinction between protein folding and aggregation: aggregation can be controlled by affecting the intermolecular interactions for aggregation, independently of the intramolecular interactions for protein folding. Aggregation is beyond protein folding. A unifying model that can conceptually reconcile and underlie the seemingly contradictory observations is described here. This simple principle highlights, in particular, the importance of intermolecular repulsive forces against aggregation, the magnitude of which can be correlated with the size and surface properties of molecules. The intermolecular repulsive forces generated by the common intrinsic properties of cellular macromolecules including chaperones, such as their large excluded volume and surface charges, can play a key role in preventing the aggregation of their physically connected polypeptides, thus underlying the generic intrinsic chaperone activity of soluble cellular macromolecules. Such intermolecular repulsive forces of bulky cellular macromolecules, distinct from protein conformational change and attractive interactions, could be the puzzle pieces for properly understanding the combined cellular protein folding and aggregation including how proteins can overcome their metastability to amyloid fibrils in vivo.

Keywords: Protein folding, aggregation, macromolecules, intermolecular repulsive forces, excluded volume, charges, chaperones, metastability.

[1]
Choi, S.I.; Kwon, S.; Son, A.; Jeong, H.; Kim, K.H.; Seong, B.L. Protein folding in vivo revisited. Curr. Protein Pept. Sci., 2013, 14(8), 721-733.
[http://dx.doi.org/10.2174/138920371408131227170544] [PMID: 24384034]
[2]
Baldwin, A.J.; Knowles, T.P.; Tartaglia, G.G.; Fitzpatrick, A.W.; Devlin, G.L.; Shammas, S.L.; Waudby, C.A.; Mossuto, M.F.; Meehan, S.; Gras, S.L.; Christodoulou, J.; Anthony-Cahill, S.J.; Barker, P.D.; Vendruscolo, M.; Dobson, C.M. Metastability of native proteins and the phenomenon of amyloid formation. J. Am. Chem. Soc., 2011, 133(36), 14160-14163.
[http://dx.doi.org/10.1021/ja2017703] [PMID: 21650202]
[3]
Balchin, D.; Hayer-Hartl, M.; Hartl, F.U. in vivo aspects of protein folding and quality control. Science, 2016, 353(6294) aac4354
[http://dx.doi.org/10.1126/science.aac4354] [PMID: 27365453]
[4]
Anfinsen, C.B. Principles that govern the folding of protein chains. Science, 1973, 181(4096), 223-230.
[http://dx.doi.org/10.1126/science.181.4096.223] [PMID: 4124164]
[5]
Fersht, A.R.; Matouschek, A.; Serrano, L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol., 1992, 224(3), 771-782.
[http://dx.doi.org/10.1016/0022-2836(92)90561-W] [PMID: 1569556]
[6]
Dill, K.A. Dominant forces in protein folding. Biochemistry, 1990, 29(31), 7133-7155.
[http://dx.doi.org/10.1021/bi00483a001] [PMID: 2207096]
[7]
Onuchic, J.N.; Luthey-Schulten, Z.; Wolynes, P.G. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem., 1997, 48, 545-600.
[http://dx.doi.org/10.1146/annurev.physchem.48.1.545] [PMID: 9348663]
[8]
Lyubarev, A.E.; Kurganov, B.I. Modeling of irreversible thermal protein denaturation at varying temperature. II. The complete kinetic model of Lumry and Eyring. Biochemistry (Mosc.), 1999, 64(7), 832-838.
[PMID: 10424909]
[9]
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(8), 10368-10386.
[http://dx.doi.org/10.3390/ijms130810368] [PMID: 22949867]
[10]
Kwon, S.B.; Ryu, K.; Son, A.; Jeong, H.; Lim, K.H.; Kim, K.H.; Seong, B.L.; Choi, S.I. Conversion of a soluble protein into a potent chaperone in vivo. Sci. Rep., 2019, 9(1), 2735.
[http://dx.doi.org/10.1038/s41598-019-39158-6] [PMID: 30804538]
[11]
Vendruscolo, M. Proteome folding and aggregation. Curr. Opin. Struct. Biol., 2012, 22(2), 138-143.
[http://dx.doi.org/10.1016/j.sbi.2012.01.005] [PMID: 22317916]
[12]
Lawrence, M.S.; Phillips, K.J.; Liu, D.R. Supercharging proteins can impart unusual resilience. J. Am. Chem. Soc., 2007, 129(33), 10110-10112.
[http://dx.doi.org/10.1021/ja071641y] [PMID: 17665911]
[13]
Simeonov, P.; Zahn, M.; Sträter, N.; Zuchner, T. Crystal structure of a supercharged variant of the human enteropeptidase light chain. Proteins, 2012, 80(7), 1907-1910.
[http://dx.doi.org/10.1002/prot.24084] [PMID: 22488687]
[14]
Kurnik, M.; Hedberg, L.; Danielsson, J.; Oliveberg, M. Folding without charges. Proc. Natl. Acad. Sci. USA, 2012, 109(15), 5705-5710.
[http://dx.doi.org/10.1073/pnas.1118640109] [PMID: 22454493]
[15]
Hartl, F.U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 2002, 295(5561), 1852-1858.
[http://dx.doi.org/10.1126/science.1068408] [PMID: 11884745]
[16]
Ellis, R.J. Molecular chaperones: inside and outside the Anfinsen cage. Curr. Biol., 2001, 11(24), R1038-R1040.
[http://dx.doi.org/10.1016/S0960-9822(01)00620-0] [PMID: 11747844]
[17]
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(2), 199-209.
[http://dx.doi.org/10.1016/S0092-8674(04)00299-5] [PMID: 15084258]
[18]
Apetri, A.C.; Horwich, A.L. Chaperonin chamber accelerates protein folding through passive action of preventing aggregation. Proc. Natl. Acad. Sci. USA, 2008, 105(45), 17351-17355.
[http://dx.doi.org/10.1073/pnas.0809794105] [PMID: 18987317]
[19]
Marchenko, N.Y.; Marchenkov, V.V.; Semisotnov, G.V.; Finkelstein, A.V. Strict experimental evidence that apo-chaperonin GroEL does not accelerate protein folding, although it does accelerate one of its steps. Proc. Natl. Acad. Sci. USA, 2015, 112(50), E6831-E6832.
[http://dx.doi.org/10.1073/pnas.1517712112] [PMID: 26604318]
[20]
Gupta, A.J.; Haldar, S.; Miličić, G.; Hartl, F.U.; Hayer-Hartl, M. Active cage mechanism of chaperonin-assisted protein folding demonstrated at single-molecule level. J. Mol. Biol., 2014, 426(15), 2739-2754.
[http://dx.doi.org/10.1016/j.jmb.2014.04.018] [PMID: 24816391]
[21]
Georgescauld, F.; Popova, K.; Gupta, A.J.; Bracher, A.; Engen, J.R.; Hayer-Hartl, M.; Hartl, F.U. GroEL/ES chaperonin modulates the mechanism and accelerates the rate of TIM-barrel domain folding. Cell, 2014, 157(4), 922-934.
[http://dx.doi.org/10.1016/j.cell.2014.03.038] [PMID: 24813614]
[22]
Libich, D.S.; Tugarinov, V.; Clore, G.M. Intrinsic unfoldase/foldase activity of the chaperonin GroEL directly demonstrated using multinuclear relaxation-based NMR. Proc. Natl. Acad. Sci. USA, 2015, 112(29), 8817-8823.
[http://dx.doi.org/10.1073/pnas.1510083112] [PMID: 26124125]
[23]
Luck, K.; Sheynkman, G.M.; Zhang, I.; Vidal, M. Proteome-scale human interactomics. Trends Biochem. Sci., 2017, 42(5), 342-354.
[http://dx.doi.org/10.1016/j.tibs.2017.02.006] [PMID: 28284537]
[24]
Ward, J.J.; Sodhi, J.S.; McGuffin, L.J.; Buxton, B.F.; Jones, D.T. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol., 2004, 337(3), 635-645.
[http://dx.doi.org/10.1016/j.jmb.2004.02.002] [PMID: 15019783]
[25]
Uversky, V.N.; Gillespie, J.R.; Fink, A.L. Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins, 2000, 41(3), 415-427.
[http://dx.doi.org/10.1002/1097-0134(20001115)41:3<415:AID-PROT130>3.0.CO;2-7] [PMID: 11025552]
[26]
Thirumalai, D.; Reddy, G. Protein thermodynamics: Are native proteins metastable? Nat. Chem., 2011, 3(12), 910-911.
[http://dx.doi.org/10.1038/nchem.1207] [PMID: 22109266]
[27]
Guijarro, J.I.; Sunde, M.; Jones, J.A.; Campbell, I.D.; Dobson, C.M. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. USA, 1998, 95(8), 4224-4228.
[http://dx.doi.org/10.1073/pnas.95.8.4224] [PMID: 9539718]
[28]
Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem., 2006, 75, 333-366.
[http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901] [PMID: 16756495]
[29]
Marinelli, P.; Navarro, S.; Baño-Polo, M.; Morel, B.; Graña-Montes, R.; Sabe, A.; Canals, F.; Fernandez, M.R.; Conejero-Lara, F.; Ventura, S. Global protein stabilization does not suffice to prevent amyloid fibril formation. ACS Chem. Biol., 2018, 13(8), 2094-2105.
[http://dx.doi.org/10.1021/acschembio.8b00607] [PMID: 29966079]
[30]
Olzscha, H.; Schermann, S.M.; Woerner, A.C.; Pinkert, S.; Hecht, M.H.; Tartaglia, G.G.; Vendruscolo, M.; Hayer-Hartl, M.; Hartl, F.U.; Vabulas, R.M. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell, 2011, 144(1), 67-78.
[http://dx.doi.org/10.1016/j.cell.2010.11.050] [PMID: 21215370]
[31]
Ciryam, P.; Kundra, R.; Morimoto, R.I.; Dobson, C.M.; Vendruscolo, M. Supersaturation is a major driving force for protein aggregation in neurodegenerative diseases. Trends Pharmacol. Sci., 2015, 36(2), 72-77.
[http://dx.doi.org/10.1016/j.tips.2014.12.004] [PMID: 25636813]
[32]
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(1), 74-79.
[http://dx.doi.org/10.1016/j.bbrc.2008.05.186] [PMID: 18555007]
[33]
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(4), 635-643.
[http://dx.doi.org/10.1110/ps.062330907] [PMID: 17384228]
[34]
Paraskevopoulou, V.; Falcone, F.H. Polyionic tags as enhancers of protein solubility in recombinant protein expression. Microorganisms, 2018, 6(2), 47.
[http://dx.doi.org/10.3390/microorganisms6020047] [PMID: 29882886]
[35]
Zhou, H.X.; Pang, X. Electrostatic interactions in protein structure, folding, binding, and condensation. Chem. Rev., 2018, 118(4), 1691-1741.
[http://dx.doi.org/10.1021/acs.chemrev.7b00305] [PMID: 29319301]
[36]
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(18), 9907-9912.
[http://dx.doi.org/10.1073/pnas.160086297] [PMID: 10944185]
[37]
Olsen, S.N.; Andersen, K.B.; Randolph, T.W.; Carpenter, J.F.; Westh, P. Role of electrostatic repulsion on colloidal stability of Bacillus halmapalus alpha-amylase. Biochim. Biophys. Acta, 2009, 1794(7), 1058-1065.
[http://dx.doi.org/10.1016/j.bbapap.2009.02.010] [PMID: 19281873]
[38]
Ortega-Vinuesa, J.L.; Marten-Rodriguez, A.; Hidalgo-Alvarez, R. Colloidal stability of polymer colloids with different interfacial properties: Mechanisms. J. Colloid Interface Sci., 1996, 184(1), 259-267.
[http://dx.doi.org/10.1006/jcis.1996.0619] [PMID: 8954662]
[39]
Taketomi, H.; Ueda, Y.; Gō, N. Studies on protein folding, unfolding and fluctuations by computer simulation. I. The effect of specific amino acid sequence represented by specific inter-unit interactions. Int. J. Pept. Protein Res., 1975, 7(6), 445-459.
[http://dx.doi.org/10.1111/j.1399-3011.1975.tb02465.x] [PMID: 1201909]
[40]
Bryngelson, J.D.; Wolynes, P.G. Spin glasses and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. USA, 1987, 84(21), 7524-7528.
[http://dx.doi.org/10.1073/pnas.84.21.7524] [PMID: 3478708]
[41]
Best, R.B.; Hummer, G.; Eaton, W.A. Native contacts determine protein folding mechanisms in atomistic simulations. Proc. Natl. Acad. Sci. USA, 2013, 110(44), 17874-17879.
[http://dx.doi.org/10.1073/pnas.1311599110] [PMID: 24128758]
[42]
Fink, A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des., 1998, 3(1), R9-R23.
[http://dx.doi.org/10.1016/S1359-0278(98)00002-9] [PMID: 9502314]
[43]
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(10), 1283-1287.
[http://dx.doi.org/10.1038/nbt1096-1283] [PMID: 9631094]
[44]
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(23), 13060-13065.
[http://dx.doi.org/10.1073/pnas.181479798] [PMID: 11687604]
[45]
Morell, M.; Bravo, R.; Espargaró, A.; Sisquella, X.; Avilés, F.X.; Fernàndez-Busquets, X.; Ventura, S. Inclusion bodies: specificity in their aggregation process and amyloid-like structure. Biochim. Biophys. Acta, 2008, 1783(10), 1815-1825.
[http://dx.doi.org/10.1016/j.bbamcr.2008.06.007] [PMID: 18619498]
[46]
Ellis, R.J.; Hartl, F.U. Principles of protein folding in the cellular environment. Curr. Opin. Struct. Biol., 1999, 9(1), 102-110.
[http://dx.doi.org/10.1016/S0959-440X(99)80013-X] [PMID: 10047582]
[47]
Maier, T.; Ferbitz, L.; Deuerling, E.; Ban, N. A cradle for new proteins: trigger factor at the ribosome. Curr. Opin. Struct. Biol., 2005, 15(2), 204-212.
[http://dx.doi.org/10.1016/j.sbi.2005.03.005] [PMID: 15837180]
[48]
Schimmele, B.; Gräfe, N.; Plückthun, A. Ribosome display of mammalian receptor domains. Protein Eng. Des. Sel., 2005, 18(6), 285-294.
[http://dx.doi.org/10.1093/protein/gzi030] [PMID: 15932906]
[49]
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(3), 715-719.
[http://dx.doi.org/10.1016/j.bbrc.2004.05.081] [PMID: 15184041]
[50]
Brandt, F.; Etchells, S.A.; Ortiz, J.O.; Elcock, A.H.; Hartl, F.U.; Baumeister, W. The native 3D organization of bacterial polysomes. Cell, 2009, 136(2), 261-271.
[http://dx.doi.org/10.1016/j.cell.2008.11.016] [PMID: 19167328]
[51]
Kaiser, C.M.; Goldman, D.H.; Chodera, J.D.; Tinoco, I., Jr; Bustamante, C. The ribosome modulates nascent protein folding. Science, 2011, 334(6063), 1723-1727.
[http://dx.doi.org/10.1126/science.1209740] [PMID: 22194581]
[52]
Choi, S.I.; Ryu, K.; Seong, B.L. RNA-mediated chaperone type for de novo protein folding. RNA Biol., 2009, 6(1), 21-24.
[http://dx.doi.org/10.4161/rna.6.1.7441] [PMID: 19106620]
[53]
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(2), 207-216.
[http://dx.doi.org/10.1016/j.pep.2004.04.020] [PMID: 15249042]
[54]
Samelson, A.J.; Jensen, M.K.; Soto, R.A.; Cate, J.H.; Marqusee, S. Quantitative determination of ribosome nascent chain stability. Proc. Natl. Acad. Sci. USA, 2016, 113(47), 13402-13407.
[http://dx.doi.org/10.1073/pnas.1610272113] [PMID: 27821780]
[55]
Lang, L.; Zetterström, P.; Brännström, T.; Marklund, S.L.; Danielsson, J.; Oliveberg, M. SOD1 aggregation in ALS mice shows simplistic test tube behavior. Proc. Natl. Acad. Sci. USA, 2015, 112(32), 9878-9883.
[http://dx.doi.org/10.1073/pnas.1503328112] [PMID: 26221023]
[56]
Zhou, A.Q.; O’Hern, C.S.; Regan, L. Revisiting the Ramachandran plot from a new angle. Protein Sci., 2011, 20(7), 1166-1171.
[http://dx.doi.org/10.1002/pro.644] [PMID: 21538644]
[57]
Lammert, H.; Wolynes, P.G.; Onuchic, J.N. The role of atomic level steric effects and attractive forces in protein folding. Proteins, 2012, 80(2), 362-373.
[http://dx.doi.org/10.1002/prot.23187] [PMID: 22081451]
[58]
Radley, T.L.; Markowska, A.I.; Bettinger, B.T.; Ha, J.H.; Loh, S.N. Allosteric switching by mutually exclusive folding of protein domains. J. Mol. Biol., 2003, 332(3), 529-536.
[http://dx.doi.org/10.1016/S0022-2836(03)00925-2] [PMID: 12963365]
[59]
Choi, S.I.; Lim, K.H.; Seong, B.L. Chaperoning roles of macromolecules interacting with proteins in vivo. Int. J. Mol. Sci., 2011, 12(3), 1979-1990.
[http://dx.doi.org/10.3390/ijms12031979] [PMID: 21673934]
[60]
Randles, L.G.; Batey, S.; Steward, A.; Clarke, J. Distinguishing specific and nonspecific interdomain interactions in multidomain proteins. Biophys. J., 2008, 94(2), 622-628.
[http://dx.doi.org/10.1529/biophysj.107.119123] [PMID: 17890397]
[61]
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(37), 7250-7262.
[http://dx.doi.org/10.1021/bi300653m] [PMID: 22924672]
[62]
Graña-Montes, R.; Marinelli, P.; Reverter, D.; Ventura, S. N-terminal protein tails act as aggregation protective entropic bristles: the SUMO case. Biomacromolecules, 2014, 15(4), 1194-1203.
[http://dx.doi.org/10.1021/bm401776z] [PMID: 24564702]
[63]
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.
[http://dx.doi.org/10.1146/annurev.biophys.37.032807.125817] [PMID: 18573087]
[64]
Ellis, R.J. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol., 2001, 11(1), 114-119.
[http://dx.doi.org/10.1016/S0959-440X(00)00172-X] [PMID: 11179900]
[65]
Marenduzzo, D.; Finan, K.; Cook, P.R. The depletion attraction: an underappreciated force driving cellular organization. J. Cell Biol., 2006, 175(5), 681-686.
[http://dx.doi.org/10.1083/jcb.200609066] [PMID: 17145959]
[66]
Ai, X.; Zhou, Z.; Bai, Y.; Choy, W.Y. 15N NMR spin relaxation dispersion study of the molecular crowding effects on protein folding under native conditions. J. Am. Chem. Soc., 2006, 128(12), 3916-3917.
[http://dx.doi.org/10.1021/ja057832n] [PMID: 16551092]
[67]
Hagai, T.; Levy, Y. Ubiquitin not only serves as a tag but also assists degradation by inducing protein unfolding. Proc. Natl. Acad. Sci. USA, 2010, 107(5), 2001-2006.
[http://dx.doi.org/10.1073/pnas.0912335107] [PMID: 20080694]
[68]
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(16), 6166-6171.
[http://dx.doi.org/10.1073/pnas.0510496103] [PMID: 16606842]
[69]
Arviv, O.; Levy, Y. Folding of multidomain proteins: biophysical consequences of tethering even in apparently independent folding. Proteins, 2012, 80(12), 2780-2798.
[http://dx.doi.org/10.1002/prot.24161] [PMID: 22890725]
[70]
Sarkar, M.; Li, C.; Pielak, G.J. Soft interactions and crowding. Biophys. Rev., 2013, 5(2), 187-194.
[http://dx.doi.org/10.1007/s12551-013-0104-4] [PMID: 28510157]
[71]
Danielsson, J.; Mu, X.; Lang, L.; Wang, H.; Binolfi, A.; Theillet, F.X.; Bekei, B.; Logan, D.T.; Selenko, P.; Wennerström, H.; Oliveberg, M. Thermodynamics of protein destabilization in live cells. Proc. Natl. Acad. Sci. USA, 2015, 112(40), 12402-12407.
[http://dx.doi.org/10.1073/pnas.1511308112] [PMID: 26392565]
[72]
Tsai, M.Y.; Zheng, W.; Balamurugan, D.; Schafer, N.P.; Kim, B.L.; Cheung, M.S.; Wolynes, P.G. Electrostatics, structure prediction, and the energy landscapes for protein folding and binding. Protein Sci., 2016, 25(1), 255-269.
[http://dx.doi.org/10.1002/pro.2751] [PMID: 26183799]
[73]
Fersht, A.R. Conformational equilibria in -and -chymotrypsin. The energetics and importance of the salt bridge. J. Mol. Biol., 1972, 64(2), 497-509.
[http://dx.doi.org/10.1016/0022-2836(72)90513-X] [PMID: 5023185]
[74]
Honig, B.H.; Hubbell, W.L. Stability of “salt bridges” in membrane proteins. Proc. Natl. Acad. Sci. USA, 1984, 81(17), 5412-5416.
[http://dx.doi.org/10.1073/pnas.81.17.5412] [PMID: 6591197]
[75]
Honig, B.H.; Hubbell, W.L.; Flewelling, R.F. Electrostatic interactions in membranes and proteins. Annu. Rev. Biophys. Biophys. Chem., 1986, 15, 163-193.
[http://dx.doi.org/10.1146/annurev.bb.15.060186.001115] [PMID: 2424473]
[76]
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(6), 1206-1215.
[http://dx.doi.org/10.1110/ps.440101] [PMID: 11369859]
[77]
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(Suppl. 4), 16419-16426.
[http://dx.doi.org/10.1073/pnas.212527999] [PMID: 12374855]
[78]
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(6950), 805-808.
[http://dx.doi.org/10.1038/nature01891] [PMID: 12917692]
[79]
Sandelin, E.; Nordlund, A.; Andersen, P.M.; Marklund, S.S.; Oliveberg, M. Amyotrophic lateral sclerosis-associated copper/zinc superoxide dismutase mutations preferentially reduce the repulsive charge of the proteins. J. Biol. Chem., 2007, 282(29), 21230-21236.
[http://dx.doi.org/10.1074/jbc.M700765200] [PMID: 17513298]
[80]
LaVallie, E.R.; Lu, Z.; Diblasio-Smith, E.A.; Collins-Racie, L.A.; McCoy, J.M. Thioredoxin as a fusion partner for production of soluble recombinant proteins in Escherichia coli. Methods Enzymol., 2000, 326, 322-340.
[http://dx.doi.org/10.1016/S0076-6879(00)26063-1] [PMID: 11036651]
[81]
Wilkinson, D.L.; Harrison, R.G. Predicting the solubility of recombinant proteins in Escherichia coli. Biotechnology (N. Y.), 1991, 9(5), 443-448.
[PMID: 1367308]
[82]
Jones, L.S.; Yazzie, B.; Middaugh, C.R. Polyanions and the proteome. Mol. Cell. Proteomics, 2004, 3(8), 746-769.
[http://dx.doi.org/10.1074/mcp.R400008-MCP200] [PMID: 15143156]
[83]
Farías-Rico, J.A.; Ruud Selin, F.; Myronidi, I.; Frühauf, M.; von Heijne, G. Effects of protein size, thermodynamic stability, and net charge on cotranslational folding on the ribosome. Proc. Natl. Acad. Sci. USA, 2018, 115(40), E9280-E9287.
[http://dx.doi.org/10.1073/pnas.1812756115] [PMID: 30224455]
[84]
Marino, J.; Buholzer, K.J.; Zosel, F.; Nettels, D.; Schuler, B. Charge interactions can dominate coupled folding and binding on the ribosome. Biophys. J., 2018, 115(6), 996-1006.
[http://dx.doi.org/10.1016/j.bpj.2018.07.037] [PMID: 30173887]
[85]
Pappenberger, G.; McCormack, E.A.; Willison, K.R. Quantitative actin folding reactions using yeast CCT purified via an internal tag in the CCT3/gamma subunit. J. Mol. Biol., 2006, 360(2), 484-496.
[http://dx.doi.org/10.1016/j.jmb.2006.05.003] [PMID: 16762366]
[86]
Patzelt, H.; Rüdiger, S.; Brehmer, D.; Kramer, G.; Vorderwülbecke, S.; Schaffitzel, E.; Waitz, A.; Hesterkamp, T.; Dong, L.; Schneider-Mergener, J.; Bukau, B.; Deuerling, E. Binding specificity of Escherichia coli trigger factor. Proc. Natl. Acad. Sci. USA, 2001, 98(25), 14244-14249.
[http://dx.doi.org/10.1073/pnas.261432298] [PMID: 11724963]
[87]
Koldewey, P.; Stull, F.; Horowitz, S.; Martin, R.; Bardwell, J.C.A. Forces driving chaperone action. Cell, 2016, 166(2), 369-379.
[http://dx.doi.org/10.1016/j.cell.2016.05.054] [PMID: 27293188]
[88]
Horowitz, S.; Koldewey, P.; Stull, F.; Bardwell, J.C. Folding while bound to chaperones. Curr. Opin. Struct. Biol., 2018, 48, 1-5.
[http://dx.doi.org/10.1016/j.sbi.2017.06.009] [PMID: 28734135]
[89]
Mu, X.; Choi, S.; Lang, L.; Mowray, D.; Dokholyan, N.V.; Danielsson, J.; Oliveberg, M. Physicochemical code for quinary protein interactions in Escherichia coli. Proc. Natl. Acad. Sci. USA, 2017, 114(23), E4556-E4563.
[http://dx.doi.org/10.1073/pnas.1621227114] [PMID: 28536196]
[90]
Kim, H.K.; Choi, S.I.; Seong, B.L. 5S rRNA-assisted DnaK refolding. Biochem. Biophys. Res. Commun., 2010, 391(2), 1177-1181.
[http://dx.doi.org/10.1016/j.bbrc.2009.11.176] [PMID: 19962961]
[91]
Gray, M.J.; Wholey, W.Y.; Wagner, N.O.; Cremers, C.M.; Mueller-Schickert, A.; Hock, N.T.; Krieger, A.G.; Smith, E.M.; Bender, R.A.; Bardwell, J.C.; Jakob, U. Polyphosphate is a primordial chaperone. Mol. Cell, 2014, 53(5), 689-699.
[http://dx.doi.org/10.1016/j.molcel.2014.01.012] [PMID: 24560923]
[92]
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(7), 1501-1507.
[http://dx.doi.org/10.1093/emboj/16.7.1501] [PMID: 9130695]
[93]
Wayne, N.; Bolon, D.N. Charge-rich regions modulate the anti-aggregation activity of Hsp90. J. Mol. Biol., 2010, 401(5), 931-939.
[http://dx.doi.org/10.1016/j.jmb.2010.06.066] [PMID: 20615417]
[94]
Richarme, G.; Kohiyama, M. Amino acid specificity of the Escherichia coli chaperone GroEL (heat shock protein 60). J. Biol. Chem., 1994, 269(10), 7095-7098.
[PMID: 7907325]
[95]
Pappenberger, G.; Wilsher, J.A.; Roe, S.M.; Counsell, D.J.; Willison, K.R.; Pearl, L.H. Crystal structure of the CCTgamma apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J. Mol. Biol., 2002, 318(5), 1367-1379.
[http://dx.doi.org/10.1016/S0022-2836(02)00190-0] [PMID: 12083524]
[96]
Ellgaard, L.; Helenius, A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol., 2003, 4(3), 181-191.
[http://dx.doi.org/10.1038/nrm1052] [PMID: 12612637]
[97]
Uhlén, M.; Fagerberg, L.; Hallström, B.M.; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, Å.; Kampf, C.; Sjöstedt, E.; Asplund, A.; Olsson, I.; Edlund, K.; Lundberg, E.; Navani, S.; Szigyarto, C.A.; Odeberg, J.; Djureinovic, D.; Takanen, J.O.; Hober, S.; Alm, T.; Edqvist, P.H.; Berling, H.; Tegel, H.; Mulder, J.; Rockberg, J.; Nilsson, P.; Schwenk, J.M.; Hamsten, M.; von Feilitzen, K.; Forsberg, M.; Persson, L.; Johansson, F.; Zwahlen, M.; von Heijne, G.; Nielsen, J.; Pontén, F. Proteomics. Tissue-based map of the human proteome. Science, 2015, 347(6220)1260419
[http://dx.doi.org/10.1126/science.1260419] [PMID: 25613900]
[98]
Chothia, C.; Gough, J.; Vogel, C.; Teichmann, S.A. Evolution of the protein repertoire. Science, 2003, 300(5626), 1701-1703.
[http://dx.doi.org/10.1126/science.1085371] [PMID: 12805536]
[99]
Holtkamp, W.; Kokic, G.; Jäger, M.; Mittelstaet, J.; Komar, A.A.; Rodnina, M.V. Cotranslational protein folding on the ribosome monitored in real time. Science, 2015, 350(6264), 1104-1107.
[http://dx.doi.org/10.1126/science.aad0344] [PMID: 26612953]
[100]
Cabrita, L.D.; Cassaignau, A.M.E.; Launay, H.M.M.; Waudby, C.A.; Wlodarski, T.; Camilloni, C.; Karyadi, M.E.; Robertson, A.L.; Wang, X.; Wentink, A.S.; Goodsell, L.; Woolhead, C.A.; Vendruscolo, M.; Dobson, C.M.; Christodoulou, J. A structural ensemble of a ribosome-nascent chain complex during cotranslational protein folding. Nat. Struct. Mol. Biol., 2016, 23(4), 278-285.
[http://dx.doi.org/10.1038/nsmb.3182] [PMID: 26926436]
[101]
Nilsson, O.B.; Hedman, R.; Marino, J.; Wickles, S.; Bischoff, L.; Johansson, M.; Müller-Lucks, A.; Trovato, F.; Puglisi, J.D.; O’Brien, E.P.; Beckmann, R.; von Heijne, G. Cotranslational protein folding inside the ribosome exit tunnel. Cell Rep., 2015, 12(10), 1533-1540.
[http://dx.doi.org/10.1016/j.celrep.2015.07.065] [PMID: 26321634]
[102]
Waugh, D.S. Making the most of affinity tags. Trends Biotechnol., 2005, 23(6), 316-320.
[http://dx.doi.org/10.1016/j.tibtech.2005.03.012] [PMID: 15922084]
[103]
Wittrup, K.D. Protein engineering by cell-surface display. Curr. Opin. Biotechnol., 2001, 12(4), 395-399.
[http://dx.doi.org/10.1016/S0958-1669(00)00233-0] [PMID: 11551469]
[104]
Kapust, R.B.; Waugh, D.S. Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci., 1999, 8(8), 1668-1674.
[http://dx.doi.org/10.1110/ps.8.8.1668] [PMID: 10452611]
[105]
Jurado, P.; de Lorenzo, V.; Fernández, L.A. Thioredoxin fusions increase folding of single chain Fv antibodies in the cytoplasm of Escherichia coli: evidence that chaperone activity is the prime effect of thioredoxin. J. Mol. Biol., 2006, 357(1), 49-61.
[http://dx.doi.org/10.1016/j.jmb.2005.12.058] [PMID: 16427080]
[106]
Kudlicki, W.; Coffman, A.; Kramer, G.; Hardesty, B. Ribosomes and ribosomal RNA as chaperones for folding of proteins. Fold. Des., 1997, 2(2), 101-108.
[http://dx.doi.org/10.1016/S1359-0278(97)00014-X] [PMID: 9135982]
[107]
Das, D.; Das, A.; Samanta, D.; Ghosh, J.; Dasgupta, S.; Bhattacharya, A.; Basu, A.; Sanyal, S.; Das Gupta, C. Role of the ribosome in protein folding. Biotechnol. J., 2008, 3(8), 999-1009.
[http://dx.doi.org/10.1002/biot.200800098] [PMID: 18702035]
[108]
Frydman, J.; Erdjument-Bromage, H.; Tempst, P.; 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(7), 697-705.
[http://dx.doi.org/10.1038/10754] [PMID: 10404229]
[109]
Sokolovski, M.; Bhattacherjee, A.; Kessler, N.; Levy, Y.; Horovitz, A. Thermodynamic protein destabilization by GFP tagging: A case of interdomain allostery. Biophys. J., 2015, 109(6), 1157-1162.
[http://dx.doi.org/10.1016/j.bpj.2015.04.032] [PMID: 25998254]
[110]
Dave, K.; Gelman, H.; Thu, C.T.; Guin, D.; Gruebele, M. The effect of fluorescent protein tags on phosphoglycerate kinase stability is nonadditive. J. Phys. Chem. B, 2016, 120(11), 2878-2885.
[http://dx.doi.org/10.1021/acs.jpcb.5b11915] [PMID: 26923443]
[111]
Batey, S.; Clarke, J. The folding pathway of a single domain in a multidomain protein is not affected by its neighbouring domain. J. Mol. Biol., 2008, 378(2), 297-301.
[http://dx.doi.org/10.1016/j.jmb.2008.02.032] [PMID: 18371978]
[112]
Tian, P.; Steward, A.; Kudva, R.; Su, T.; Shilling, P.J.; Nickson, A.A.; Hollins, J.J.; Beckmann, R.; von Heijne, G.; Clarke, J.; Best, R.B. Folding pathway of an Ig domain is conserved on and off the ribosome. Proc. Natl. Acad. Sci. USA, 2018, 115(48), E11284-E11293.
[http://dx.doi.org/10.1073/pnas.1810523115] [PMID: 30413621]
[113]
Kardos, J.; Yamamoto, K.; Hasegawa, K.; Naiki, H.; Goto, Y. Direct measurement of the thermodynamic parameters of amyloid formation by isothermal titration calorimetry. J. Biol. Chem., 2004, 279(53), 55308-55314.
[http://dx.doi.org/10.1074/jbc.M409677200] [PMID: 15494406]
[114]
O’Nuallain, B.; Shivaprasad, S.; Kheterpal, I.; Wetzel, R. Thermodynamics of A beta(1-40) amyloid fibril elongation. Biochemistry, 2005, 44(38), 12709-12718.
[http://dx.doi.org/10.1021/bi050927h] [PMID: 16171385]
[115]
Carulla, N.; Caddy, G.L.; Hall, D.R.; Zurdo, J.; Gairí, M.; Feliz, M.; Giralt, E.; Robinson, C.V.; Dobson, C.M. Molecular recycling within amyloid fibrils. Nature, 2005, 436(7050), 554-558.
[http://dx.doi.org/10.1038/nature03986] [PMID: 16049488]
[116]
Butt, T.R.; Jonnalagadda, S.; Monia, B.P.; Sternberg, E.J.; Marsh, J.A.; Stadel, J.M.; Ecker, D.J.; Crooke, S.T. Ubiquitin fusion augments the yield of cloned gene products in Escherichia coli. Proc. Natl. Acad. Sci. USA, 1989, 86(8), 2540-2544.
[http://dx.doi.org/10.1073/pnas.86.8.2540] [PMID: 2539593]
[117]
Butt, T.R.; Edavettal, S.C.; Hall, J.P.; Mattern, M.R. SUMO fusion technology for difficult-to-express proteins. Protein Expr. Purif., 2005, 43(1), 1-9.
[http://dx.doi.org/10.1016/j.pep.2005.03.016] [PMID: 16084395]
[118]
Kronqvist, N.; Sarr, M.; Lindqvist, A.; Nordling, K.; Otikovs, M.; Venturi, L.; Pioselli, B.; Purhonen, P.; Landreh, M.; Biverstål, H.; Toleikis, Z.; Sjöberg, L.; Robinson, C.V.; Pelizzi, N.; Jörnvall, H.; Hebert, H.; Jaudzems, K.; Curstedt, T.; Rising, A.; Johansson, J. Efficient protein production inspired by how spiders make silk. Nat. Commun., 2017, 8, 15504.
[http://dx.doi.org/10.1038/ncomms15504] [PMID: 28534479]
[119]
Sarr, M.; Kronqvist, N.; Chen, G.; Aleksis, R.; Purhonen, P.; Hebert, H.; Jaudzems, K.; Rising, A.; Johansson, J. A spidroin-derived solubility tag enables controlled aggregation of a designed amyloid protein. FEBS J., 2018, 285(10), 1873-1885.
[http://dx.doi.org/10.1111/febs.14451] [PMID: 29604175]
[120]
Kramer, R.M.; Shende, V.R.; Motl, N.; Pace, C.N.; Scholtz, J.M. Toward a molecular understanding of protein solubility: increased negative surface charge correlates with increased solubility. Biophys. J., 2012, 102(8), 1907-1915.
[http://dx.doi.org/10.1016/j.bpj.2012.01.060] [PMID: 22768947]
[121]
Pouchucq, L.; Lobos-Ruiz, P.; Araya, G.; Valpuesta, J.M.; Monasterio, O. The chaperonin CCT promotes the formation of fibrillar aggregates of γ-tubulin. Biochim. Biophys. Acta. Proteins Proteomics, 2018, 1866(4), 519-526.
[http://dx.doi.org/10.1016/j.bbapap.2018.01.007] [PMID: 29339327]
[122]
Chernoff, Y.O.; Lindquist, S.L.; Ono, B.; Inge-Vechtomov, S.G.; Liebman, S.W. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor. [psi+] Science, 1995, 268(5212), 880-884.
[http://dx.doi.org/10.1126/science.7754373] [PMID: 7754373]
[123]
Falsone, S.F.; Kungl, A.J.; Rek, A.; Cappai, R.; Zangger, K. The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein alpha-synuclein. J. Biol. Chem., 2009, 284(45), 31190-31199.
[http://dx.doi.org/10.1074/jbc.M109.057240] [PMID: 19759002]
[124]
Allen, K.D.; Wegrzyn, R.D.; Chernova, T.A.; Müller, S.; Newnam, G.P.; Winslett, P.A.; Wittich, K.B.; Wilkinson, K.D.; Chernoff, Y.O. Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion. [PSI+] Genetics, 2005, 169(3), 1227-1242.
[http://dx.doi.org/10.1534/genetics.104.037168] [PMID: 15545639]
[125]
Higurashi, T.; Hines, J.K.; Sahi, C.; Aron, R.; Craig, E.A. Specificity of the J-protein Sis1 in the propagation of 3 yeast prions. Proc. Natl. Acad. Sci. USA, 2008, 105(43), 16596-16601.
[http://dx.doi.org/10.1073/pnas.0808934105] [PMID: 18955697]
[126]
Blondel, M.; Soubigou, F.; Evrard, J.; Nguyen, P.H.; Hasin, N.; Chédin, S.; Gillet, R.; Contesse, M.A.; Friocourt, G.; Stahl, G.; Jones, G.W.; Voisset, C. Protein folding activity of the ribosome is involved in yeast prion propagation. Sci. Rep., 2016, 6, 32117.
[http://dx.doi.org/10.1038/srep32117] [PMID: 27633137]
[127]
Burke, K.A.; Yates, E.A.; Legleiter, J. Biophysical insights into how surfaces, including lipid membranes, modulate protein aggregation related to neurodegeneration. Front. Neurol., 2013, 4, 17.
[http://dx.doi.org/10.3389/fneur.2013.00017] [PMID: 23459674]
[128]
Stewart, K.L.; Radford, S.E. Amyloid plaques beyond Aβ: a survey of the diverse modulators of amyloid aggregation. Biophys. Rev., 2017, 9(4), 405-419.
[http://dx.doi.org/10.1007/s12551-017-0271-9] [PMID: 28631243]
[129]
Xie, L.; Jakob, U. Inorganic polyphosphate, a multifunctional polyanionic protein scaffold. J. Biol. Chem., 2019, 294(6), 2180-2190.
[http://dx.doi.org/10.1074/jbc.REV118.002808] [PMID: 30425096]
[130]
Ma, F.H.; Li, C.; Liu, Y.; Shi, L. Mimicking molecular chaperones to regulate protein folding. Adv. Mater., 2019. e1805945
[http://dx.doi.org/10.1002/adma.201805945] [PMID: 31045287]
[131]
Yoshimura, Y.; Lin, Y.; Yagi, H.; Lee, Y.H.; Kitayama, H.; Sakurai, K.; So, M.; Ogi, H.; Naiki, H.; Goto, Y. Distinguishing crystal-like amyloid fibrils and glass-like amorphous aggregates from their kinetics of formation. Proc. Natl. Acad. Sci. USA, 2012, 109(36), 14446-14451.
[http://dx.doi.org/10.1073/pnas.1208228109] [PMID: 22908252]
[132]
Romanova, N.V.; Chernoff, Y.O. Hsp104 and prion propagation. Protein Pept. Lett., 2009, 16(6), 598-605.
[http://dx.doi.org/10.2174/092986609788490078] [PMID: 19519517]
[133]
Kovachev, P.S.; Banerjee, D.; Rangel, L.P.; Eriksson, J.; Pedrote, M.M.; Martins-Dinis, M.M.D.C.; Edwards, K.; Cordeiro, Y.; Silva, J.L.; Sanyal, S. Distinct modulatory role of RNA in the aggregation of the tumor suppressor protein p53 core domain. J. Biol. Chem., 2017, 292(22), 9345-9357.
[http://dx.doi.org/10.1074/jbc.M116.762096] [PMID: 28420731]


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