Login Register Cart 0
Review Article

从 Levinthal悖论到细胞环境扰动对蛋白质折叠的影响

卷 26, 期 42, 2019

页: [7537 - 7554] 页: 18

弟呕挨: 10.2174/0929867325666181017160857

价格: $65

摘要

背景：已知蛋白质序列的数量迅速增加，需要更有效的方法来预测蛋白质的三维（3D）结构，从而为合理的药物设计提供基础知识。了解蛋白质的折叠机制对于预测蛋白质的3D结构以及设计具有新功能和医学应用的蛋白质非常有价值。 Levinthal的悖论是，尽管即使对于100个残基的蛋白质也无法完全采样到天文数字的构象数量，但自然界中的蛋白质通常会在几微秒到几小时的时间范围内折叠成天然状态。这些矛盾的结果表明，有机物中存在可以协助蛋白质折叠的因素。 方法：在本文中，我们选择了一个拥挤的细胞状环境和温度，并选择了前三个翻译后修饰（PTM）作为示例，以表明 Levinthal的悖论不能反映蛋白质的折叠机制。然后，我们揭示了这些因素对蛋白质折叠的影响。 结果：本综述总结的结果表明，拥挤的细胞状环境，温度和前三个PTM重塑了蛋白质的自由能态（FEL），从而调节了折叠过程。熵和焓之间的平衡是了解拥挤的细胞样环境和PTM对蛋白质折叠的影响的关键。另外，蛋白质的稳定性/柔韧性受温度调节。 结论：本文得出结论，细胞环境可以直接干预蛋白质折叠。细胞环境与序列进化的长期相互作用可以使蛋白质有效折叠。因此，为了正确理解蛋白质的折叠机制，应考虑细胞环境对蛋白质折叠的影响。

关键词: 蛋白质折叠，自由能景观，拥挤的细胞状环境，环境温度，磷酸化，糖基化和乙酰化。

« Previous Next »
[1]
Katritch, V.; Cherezov, V.; Stevens, R.C. Structure-function of the G protein-coupled receptor superfamily. Annu. Rev. Pharmacol. Toxicol., 2013, 53, 531-556.
[http://dx.doi.org/10.1146/annurev-pharmtox-032112-135923] [PMID: 23140243]
[2]
Dunker, A.K.; Silman, I.; Uversky, V.N.; Sussman, J.L. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol., 2008, 18(6), 756-764.
[http://dx.doi.org/10.1016/j.sbi.2008.10.002] [PMID: 18952168]
[3]
Lindorff-Larsen, K.; Piana, S.; Dror, R.O.; Shaw, D.E. How fast-folding proteins fold. Science, 2011, 334(6055), 517-520.
[http://dx.doi.org/10.1126/science.1208351] [PMID: 22034434]
[4]
Huang, Z. Design of new molecular dynamics global minimum search protocols for mapping energy landscapes and conformations of folded polypeptides and mini-proteins, 2005.
[5]
Zeng, J.; Li, Y.; Zhang, J.Z.H.; Mei, Y. Examination of the quality of various force fields and solvation models for the equilibrium simulations of GA88 and GB88. J. Mol. Model., 2016, 22(8), 177.
[http://dx.doi.org/10.1007/s00894-016-3027-8] [PMID: 27392746]
[6]
Levinthal, C. How to fold graciously. Mossbauer Spectroscopy in Biological Systems; University of Illinois Press. Urbana, 1969, 67(41), 22-26.
[7]
Karplus, M. The Levinthal paradox: yesterday and today. Fold. Des., 1997, 2(4), S69-S75.
[http://dx.doi.org/10.1016/S1359-0278(97)00067-9] [PMID: 9269572]
[8]
Zwanzig, R.; Szabo, A.; Bagchi, B. Levinthal’s paradox. Proc. Natl. Acad. Sci. USA, 1992, 89(1), 20-22.
[http://dx.doi.org/10.1073/pnas.89.1.20] [PMID: 1729690]
[9]
Dill, K.A.; Chan, H.S. From Levinthal to pathways to funnels. Nat. Struct. Biol., 1997, 4(1), 10-19.
[http://dx.doi.org/10.1038/nsb0197-10] [PMID: 8989315]
[10]
Naganathan, A.N.; Muñoz, V. Scaling of folding times with protein size. J. Am. Chem. Soc., 2005, 127(2), 480-481.
[http://dx.doi.org/10.1021/ja044449u] [PMID: 15643845]
[11]
Wolynes, P. BIOMOLECULAR FOLDING. Moments of excitement. Science, 2016, 352(6282), 150-151.
[http://dx.doi.org/10.1126/science.aaf6626] [PMID: 27124442]
[12]
Maity, H.; Maity, M.; Krishna, M.M.; Mayne, L.; Englander, S.W. Protein folding: the stepwise assembly of foldon units. Proc. Natl. Acad. Sci. USA, 2005, 102(13), 4741-4746.
[http://dx.doi.org/10.1073/pnas.0501043102] [PMID: 15774579]
[13]
Bai, Y.; Sosnick, T.R.; Mayne, L.; Englander, S.W. Protein folding intermediates: native-state hydrogen exchange. Science, 1995, 269(5221), 192-197.
[http://dx.doi.org/10.1126/science.7618079] [PMID: 7618079]
[14]
Englander, S.W.; Mayne, L. The case for defined protein folding pathways. Proc. Natl. Acad. Sci. USA, 2017, 114(31), 8253-8258.
[http://dx.doi.org/10.1073/pnas.1706196114] [PMID: 28630329]
[15]
Baldwin, R.L. Clash between energy landscape theory and foldon-dependent protein folding. Proc. Natl. Acad. Sci. USA, 2017, 114(32), 8442-8443.
[http://dx.doi.org/10.1073/pnas.1709133114] [PMID: 28747526]
[16]
Eaton, W.A.; Wolynes, P.G. Theory, simulations, and experiments show that proteins fold by multiple pathways. Proc. Natl. Acad. Sci. USA, 2017, 114(46), E9759-E9760.
[http://dx.doi.org/10.1073/pnas.1716444114] [PMID: 29087352]
[17]
Englander, S.W.; Mayne, L. Reply to Eaton and Wolynes: How do proteins fold? Proc. Natl. Acad. Sci. USA, 2017, 114(46), E9761-E9762.
[http://dx.doi.org/10.1073/pnas.1716929114] [PMID: 29087353]
[18]
Socolich, M.; Lockless, S.W.; Russ, W.P.; Lee, H.; Gardner, K.H.; Ranganathan, R. Evolutionary information for specifying a protein fold. Nature, 2005, 437(7058), 512-518.
[http://dx.doi.org/10.1038/nature03991] [PMID: 16177782]
[19]
de Juan, D.; Pazos, F.; Valencia, A. Emerging methods in protein co-evolution. Nat. Rev. Genet., 2013, 14(4), 249-261.
[http://dx.doi.org/10.1038/nrg3414] [PMID: 23458856]
[20]
Marks, D.S.; Colwell, L.J.; Sheridan, R.; Hopf, T.A.; Pagnani, A.; Zecchina, R.; Sander, C. Protein 3D structure computed from evolutionary sequence variation. PLoS One, 2011, 6(12)e28766
[http://dx.doi.org/10.1371/journal.pone.0028766] [PMID: 22163331]
[21]
Mirny, L.A.; Abkevich, V.I.; Shakhnovich, E.I. How evolution makes proteins fold quickly. Proc. Natl. Acad. Sci. USA, 1998, 95(9), 4976-4981.
[http://dx.doi.org/10.1073/pnas.95.9.4976] [PMID: 9560213]
[22]
Theillet, F.X.; Binolfi, A.; Frembgen-Kesner, T.; Hingorani, K.; Sarkar, M.; Kyne, C.; Li, C.; Crowley, P.B.; Gierasch, L.; Pielak, G.J.; Elcock, A.H.; Gershenson, A.; Selenko, P. Physicochemical properties of cells and their effects on intrinsically disordered proteins (IDPs). Chem. Rev., 2014, 114(13), 6661-6714.
[http://dx.doi.org/10.1021/cr400695p] [PMID: 24901537]
[23]
Zhou, H.X. Influence of crowded cellular environments on protein folding, binding, and oligomerization: biological consequences and potentials of atomistic modeling. FEBS Lett., 2013, 587(8), 1053-1061.
[http://dx.doi.org/10.1016/j.febslet.2013.01.064] [PMID: 23395796]
[24]
Kuznetsova, I.M.; Turoverov, K.K.; Uversky, V.N. What macromolecular crowding can do to a protein. Int. J. Mol. Sci., 2014, 15(12), 23090-23140.
[http://dx.doi.org/10.3390/ijms151223090] [PMID: 25514413]
[25]
Zhou, Z.; Fan, J.B.; Zhu, H.L.; Shewmaker, F.; Yan, X.; Chen, X.; Chen, J.; Xiao, G.F.; Guo, L.; Liang, Y. Crowded cell-like environment accelerates the nucleation step of amyloidogenic protein misfolding. J. Biol. Chem., 2009, 284(44), 30148-30158.
[http://dx.doi.org/10.1074/jbc.M109.002832] [PMID: 19748895]
[26]
Reid, R.E.; Gariépy, J.; Saund, A.K.; Hodges, R.S. Calcium-induced protein folding. Structure-affinity relationships in synthetic analogs of the helix-loop-helix calcium binding unit. J. Biol. Chem., 1981, 256(6), 2742-2751.
[PMID: 7204374]
[27]
Hartl, F.U.; Bracher, A.; Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature, 2011, 475(7356), 324-332.
[http://dx.doi.org/10.1038/nature10317] [PMID: 21776078]
[28]
Kim, Y.E.; Hipp, M.S.; Bracher, A.; Hayer-Hartl, M.; Hartl, F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem., 2013, 82, 323-355.
[http://dx.doi.org/10.1146/annurev-biochem-060208-092442] [PMID: 23746257]
[29]
Berezovsky, I.N.; Shakhnovich, E.I. Physics and evolution of thermophilic adaptation. Proc. Natl. Acad. Sci. USA, 2005, 102(36), 12742-12747.
[http://dx.doi.org/10.1073/pnas.0503890102] [PMID: 16120678]
[30]
Karve, T.M.; Cheema, A.K. Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J. Amino Acids, 2011, 2011207691
[http://dx.doi.org/10.4061/2011/207691] [PMID: 22312457]
[31]
Khoury, G.A.; Baliban, R.C.; Floudas, C.A. Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database. Sci. Rep., 2011, 1, 90.
[http://dx.doi.org/10.1038/srep00090] [PMID: 22034591]
[32]
Scheraga, H.A.; Khalili, M.; Liwo, A. Protein-folding dynamics: overview of molecular simulation techniques. Annu. Rev. Phys. Chem., 2007, 58, 57-83.
[http://dx.doi.org/10.1146/annurev.physchem.58.032806.104614] [PMID: 17034338]
[33]
Beck, D.A.; Daggett, V. Methods for molecular dynamics simulations of protein folding/unfolding in solution. Methods, 2004, 34(1), 112-120.
[http://dx.doi.org/10.1016/j.ymeth.2004.03.008] [PMID: 15283920]
[34]
de Azevedo, W.F. Jr. Molecular dynamics simulations of protein targets identified in Mycobacterium tuberculosis. Curr. Med. Chem., 2011, 18(9), 1353-1366.
[http://dx.doi.org/10.2174/092986711795029519] [PMID: 21366529]
[35]
Bernardi, R.C.; Melo, M.C.R.; Schulten, K. Enhanced sampling techniques in molecular dynamics simulations of biological systems. Biochim. Biophys. Acta, 2015, 1850(5), 872-877.
[http://dx.doi.org/10.1016/j.bbagen.2014.10.019] [PMID: 25450171]
[36]
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]
[37]
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]
[38]
Gething, M.J.; Sambrook, J. Protein folding in the cell. Nature, 1992, 355(6355), 33-45.
[http://dx.doi.org/10.1038/355033a0] [PMID: 1731198]
[39]
Ebbinghaus, S.; Gruebele, M. Protein folding landscapes in the living cell. J. Phys. Chem. Lett., 2011, 2(4), 314-319.
[http://dx.doi.org/10.1021/jz101729z]
[40]
Zhou, H.X.; Qin, S. Simulation and modeling of crowding effects on the thermodynamic and kinetic properties of proteins with atomic details. Biophys. Rev., 2013, 5(2), 207-215.
[http://dx.doi.org/10.1007/s12551-013-0101-7] [PMID: 23710260]
[41]
Zhou, H.X. Protein folding and binding in confined spaces and in crowded solutions. J. Mol. Recognit., 2004, 17(5), 368-375.
[http://dx.doi.org/10.1002/jmr.711] [PMID: 15362094]
[42]
Qin, S.; Zhou, H.X. Generalized fundamental measure theory for atomistic modeling of macromolecular crowding. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 2010, 81(3 Pt 1)031919
[http://dx.doi.org/10.1103/PhysRevE.81.031919] [PMID: 20365782]
[43]
Qin, S.; Cai, L.; Zhou, H.X. A method for computing association rate constants of atomistically represented proteins under macromolecular crowding. Phys. Biol., 2012, 9(6)066008
[http://dx.doi.org/10.1088/1478-3975/9/6/066008] [PMID: 23197255]
[44]
Qin, S.; Minh, D.D.; McCammon, J.A.; Zhou, H.X. Method to predict crowding effects by postprocessing molecular dynamics trajectories: application to the flap dynamics of HIV-1 protease. J. Phys. Chem. Lett., 2010, 1(1), 107-110.
[http://dx.doi.org/10.1021/jz900023w] [PMID: 20228897]
[45]
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]
[46]
Tjong, H.; Zhou, H.X. The folding transition-state ensemble of a four-helix bundle protein: helix propensity as a determinant and macromolecular crowding as a probe. Biophys. J., 2010, 98(10), 2273-2280.
[http://dx.doi.org/10.1016/j.bpj.2010.01.052] [PMID: 20483336]
[47]
Batra, J.; Xu, K.; Qin, S.; Zhou, H.X. Effect of macromolecular crowding on protein binding stability: modest stabilization and significant biological consequences. Biophys. J., 2009, 97(3), 906-911.
[http://dx.doi.org/10.1016/j.bpj.2009.05.032] [PMID: 19651049]
[48]
Phillip, Y.; Harel, M.; Khait, R.; Qin, S.; Zhou, H.X.; Schreiber, G. Contrasting factors on the kinetic path to protein complex formation diminish the effects of crowding agents. Biophys. J., 2012, 103(5), 1011-1019.
[http://dx.doi.org/10.1016/j.bpj.2012.08.009] [PMID: 23009850]
[49]
Cheung, M.S.; Klimov, D.; Thirumalai, D. Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc. Natl. Acad. Sci. USA, 2005, 102(13), 4753-4758.
[http://dx.doi.org/10.1073/pnas.0409630102] [PMID: 15781864]
[50]
Minh, D.D.; Chang, C.E.; Trylska, J.; Tozzini, V.; McCammon, J.A. The influence of macromolecular crowding on HIV-1 protease internal dynamics. J. Am. Chem. Soc., 2006, 128(18), 6006-6007.
[http://dx.doi.org/10.1021/ja060483s] [PMID: 16669648]
[51]
Mittal, J.; Best, R.B. Dependence of protein folding stability and dynamics on the density and composition of macromolecular crowders. Biophys. J., 2010, 98(2), 315-320.
[http://dx.doi.org/10.1016/j.bpj.2009.10.009] [PMID: 20338853]
[52]
Homouz, D.; Perham, M.; Samiotakis, A.; Cheung, M.S.; Wittung-Stafshede, P. Crowded, cell-like environment induces shape changes in aspherical protein. Proc. Natl. Acad. Sci. USA, 2008, 105(33), 11754-11759.
[http://dx.doi.org/10.1073/pnas.0803672105] [PMID: 18697933]
[53]
Dhar, A.; Samiotakis, A.; Ebbinghaus, S.; Nienhaus, L.; Homouz, D.; Gruebele, M.; Cheung, M.S. Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding. Proc. Natl. Acad. Sci. USA, 2010, 107(41), 17586-17591.
[http://dx.doi.org/10.1073/pnas.1006760107] [PMID: 20921368]
[54]
Charlton, L.M.; Barnes, C.O.; Li, C.; Orans, J.; Young, G.B.; Pielak, G.J. Residue-level interrogation of macromolecular crowding effects on protein stability. J. Am. Chem. Soc., 2008, 130(21), 6826-6830.
[http://dx.doi.org/10.1021/ja8005995] [PMID: 18459780]
[55]
Miklos, A.C.; Sarkar, M.; Wang, Y.; Pielak, G.J. Protein crowding tunes protein stability. J. Am. Chem. Soc., 2011, 133(18), 7116-7120.
[http://dx.doi.org/10.1021/ja200067p] [PMID: 21506571]
[56]
Wang, Y.; Sarkar, M.; Smith, A.E.; Krois, A.S.; Pielak, G.J. Macromolecular crowding and protein stability. J. Am. Chem. Soc., 2012, 134(40), 16614-16618.
[http://dx.doi.org/10.1021/ja305300m] [PMID: 22954326]
[57]
Feig, M.; Sugita, Y. Variable interactions between protein crowders and biomolecular solutes are important in understanding cellular crowding. J. Phys. Chem. B, 2012, 116(1), 599-605.
[http://dx.doi.org/10.1021/jp209302e] [PMID: 22117862]
[58]
Szilágyi, A.; Závodszky, P. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure, 2000, 8(5), 493-504.
[http://dx.doi.org/10.1016/S0969-2126(00)00133-7] [PMID: 10801491]
[59]
Goldstein, R.A. Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: insights from the quasi-chemical approximation. Protein Sci., 2007, 16(9), 1887-1895.
[http://dx.doi.org/10.1110/ps.072947007] [PMID: 17766385]
[60]
Gianese, G.; Argos, P.; Pascarella, S. Structural adaptation of enzymes to low temperatures. Protein Eng., 2001, 14(3), 141-148.
[http://dx.doi.org/10.1093/protein/14.3.141] [PMID: 11342709]
[61]
D’Amico, S.; Marx, J.C.; Gerday, C.; Feller, G. Activity-stability relationships in extremophilic enzymes. J. Biol. Chem., 2003, 278(10), 7891-7896.
[http://dx.doi.org/10.1074/jbc.M212508200] [PMID: 12511577]
[62]
Meruelo, A.D.; Han, S.K.; Kim, S.; Bowie, J.U. Structural differences between thermophilic and mesophilic membrane proteins. Protein Sci., 2012, 21(11), 1746-1753.
[http://dx.doi.org/10.1002/pro.2157] [PMID: 23001966]
[63]
Georlette, D.; Blaise, V.; Collins, T.; D’Amico, S.; Gratia, E.; Hoyoux, A.; Marx, J.C.; Sonan, G.; Feller, G.; Gerday, C. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev., 2004, 28(1), 25-42.
[http://dx.doi.org/10.1016/j.femsre.2003.07.003] [PMID: 14975528]
[64]
Papaleo, E.; Pasi, M.; Riccardi, L.; Sambi, I.; Fantucci, P.; De Gioia, L. Protein flexibility in psychrophilic and mesophilic trypsins. Evidence of evolutionary conservation of protein dynamics in trypsin-like serine-proteases. FEBS Lett., 2008, 582(6), 1008-1018.
[http://dx.doi.org/10.1016/j.febslet.2008.02.048] [PMID: 18307991]
[65]
Casanueva, A.; Tuffin, M.; Cary, C.; Cowan, D.A. Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol., 2010, 18(8), 374-381.
[http://dx.doi.org/10.1016/j.tim.2010.05.002] [PMID: 20646925]
[66]
Mereghetti, P.; Riccardi, L.; Brandsdal, B.O.; Fantucci, P.; De Gioia, L.; Papaleo, E. Near native-state conformational landscape of psychrophilic and mesophilic enzymes: probing the folding funnel model. J. Phys. Chem. B, 2010, 114(22), 7609-7619.
[http://dx.doi.org/10.1021/jp911523h] [PMID: 20518574]
[67]
Åqvist, J.; Isaksen, G.V.; Brandsdal, B.O. Computation of enzyme cold adaptation. Nat. Rev.Chem., 2017, 1, 0051.
[http://dx.doi.org/10.1038/s41570-017-0051]
[68]
Bjelic, S.; Brandsdal, B.O.; Aqvist, J. Cold adaptation of enzyme reaction rates. Biochemistry, 2008, 47(38), 10049-10057.
[http://dx.doi.org/10.1021/bi801177k] [PMID: 18759500]
[69]
Isaksen, G.V.; Åqvist, J.; Brandsdal, B.O. Protein surface softness is the origin of enzyme cold-adaptation of trypsin. PLOS Comput. Biol., 2014, 10(8) e1003813
[http://dx.doi.org/10.1371/journal.pcbi.1003813] [PMID: 25165981]
[70]
Zanphorlin, L.M.; de Giuseppe, P.O.; Honorato, R.V.; Tonoli, C.C.; Fattori, J.; Crespim, E.; de Oliveira, P.S.; Ruller, R.; Murakami, M.T. Oligomerization as a strategy for cold adaptation: Structure and dynamics of the GH1 β-glucosidase from Exiguobacterium antarcticum B7. Sci. Rep., 2016, 6, 23776.
[http://dx.doi.org/10.1038/srep23776] [PMID: 27029646]
[71]
Leiros, H.K.; Willassen, N.P.; Smalås, A.O. Structural comparison of psychrophilic and mesophilic trypsins. Elucidating the molecular basis of cold-adaptation. Eur. J. Biochem., 2000, 267(4), 1039-1049.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01098.x] [PMID: 10672012]
[72]
Kumar, S.; Nussinov, R. How do thermophilic proteins deal with heat? Cell. Mol. Life Sci., 2001, 58(9), 1216-1233.
[http://dx.doi.org/10.1007/PL00000935] [PMID: 11577980]
[73]
Olufsen, M.; Smalås, A.O.; Moe, E.; Brandsdal, B.O. Increased flexibility as a strategy for cold adaptation: a comparative molecular dynamics study of cold- and warm-active uracil DNA glycosylase. J. Biol. Chem., 2005, 280(18), 18042-18048.
[http://dx.doi.org/10.1074/jbc.M500948200] [PMID: 15749696]
[74]
Olufsen, M.; Brandsdal, B.O.; Smalås, A.O. Comparative unfolding studies of psychrophilic and mesophilic uracil DNA glycosylase: MD simulations show reduced thermal stability of the cold-adapted enzyme. J. Mol. Graph. Model., 2007, 26(1), 124-134.
[http://dx.doi.org/10.1016/j.jmgm.2006.10.003] [PMID: 17134924]
[75]
Michetti, D.; Brandsdal, B.O.; Bon, D.; Isaksen, G.V.; Tiberti, M.; Papaleo, E. A comparative study of cold- and warm-adapted Endonucleases A using sequence analyses and molecular dynamics simulations. PLoS One, 2017, 12(2) e0169586
[http://dx.doi.org/10.1371/journal.pone.0169586] [PMID: 28192428]
[76]
Adekoya, O.A.; Helland, R.; Willassen, N.P.; Sylte, I. Comparative sequence and structure analysis reveal features of cold adaptation of an enzyme in the thermolysin family. Proteins, 2006, 62(2), 435-449.
[http://dx.doi.org/10.1002/prot.20773] [PMID: 16294337]
[77]
Papaleo, E.; Riccardi, L.; Villa, C.; Fantucci, P.; De Gioia, L. Flexibility and enzymatic cold-adaptation: a comparative molecular dynamics investigation of the elastase family. Biochim. Biophys. Acta, 2006, 1764(8), 1397-1406.
[http://dx.doi.org/10.1016/j.bbapap.2006.06.005] [PMID: 16920043]
[78]
Papaleo, E.; Olufsen, M.; De Gioia, L.; Brandsdal, B.O. Optimization of electrostatics as a strategy for cold-adaptation: a case study of cold- and warm-active elastases. J. Mol. Graph. Model., 2007, 26(1), 93-103.
[http://dx.doi.org/10.1016/j.jmgm.2006.09.012] [PMID: 17084098]
[79]
Papaleo, E.; Pasi, M.; Tiberti, M.; De Gioia, L. Molecular dynamics of mesophilic-like mutants of a cold-adapted enzyme: insights into distal effects induced by the mutations. PLoS One, 2011, 6(9) e24214
[http://dx.doi.org/10.1371/journal.pone.0024214] [PMID: 21915299]
[80]
Parvizpour, S.; Razmara, J.; Ramli, A.N.; Md Illias, R.; Shamsir, M.S. Structural and functional analysis of a novel psychrophilic β-mannanase from Glaciozyma antarctica PI12. J. Comput. Aided Mol. Des., 2014, 28(6), 685-698.
[http://dx.doi.org/10.1007/s10822-014-9751-1] [PMID: 24849507]
[81]
Kim, M.K.; An, Y.J.; Song, J.M.; Jeong, C.S.; Kang, M.H.; Kwon, K.K.; Lee, Y.H.; Cha, S.S. Structure-based investigation into the functional roles of the extended loop and substrate-recognition sites in an endo-β-1,4-D-mannanase from the Antarctic springtail, Cryptopygus antarcticus. Proteins, 2014, 82(11), 3217-3223.
[http://dx.doi.org/10.1002/prot.24655] [PMID: 25082572]
[82]
Gatti-Lafranconi, P.; Natalello, A.; Rehm, S.; Doglia, S.M.; Pleiss, J.; Lotti, M. Evolution of stability in a cold-active enzyme elicits specificity relaxation and highlights substrate-related effects on temperature adaptation. J. Mol. Biol., 2010, 395(1), 155-166.
[http://dx.doi.org/10.1016/j.jmb.2009.10.026] [PMID: 19850050]
[83]
Sigtryggsdóttir, A.R.; Papaleo, E.; Thorbjarnardóttir, S.H.; Kristjánsson, M.M. Flexibility of cold- and heat-adapted subtilisin-like serine proteinases evaluated with fluorescence quenching and molecular dynamics. Biochim. Biophys. Acta, 2014, 1844(4), 705-712.
[http://dx.doi.org/10.1016/j.bbapap.2014.02.009] [PMID: 24561657]
[84]
Xie, B.B.; Bian, F.; Chen, X.L.; He, H.L.; Guo, J.; Gao, X.; Zeng, Y.X.; Chen, B.; Zhou, B.C.; Zhang, Y.Z. Cold adaptation of zinc metalloproteases in the thermolysin family from deep sea and arctic sea ice bacteria revealed by catalytic and structural properties and molecular dynamics: new insights into relationship between conformational flexibility and hydrogen bonding. J. Biol. Chem., 2009, 284(14), 9257-9269.
[http://dx.doi.org/10.1074/jbc.M808421200] [PMID: 19181663]
[85]
Kovacic, F.; Mandrysch, A.; Poojari, C.; Strodel, B.; Jaeger, K.E. Structural features determining thermal adaptation of esterases. Protein Eng. Des. Sel., 2016, 29(2), 65-76.
[http://dx.doi.org/10.1093/protein/gzv061] [PMID: 26647400]
[86]
Jaenicke, R.; Böhm, G. The stability of proteins in extreme environments. Curr. Opin. Struct. Biol., 1998, 8(6), 738-748.
[http://dx.doi.org/10.1016/S0959-440X(98)80094-8] [PMID: 9914256]
[87]
Schneider, D.; Liu, Y.; Gerstein, M.; Engelman, D.M. Thermostability of membrane protein helix-helix interaction elucidated by statistical analysis. FEBS Lett., 2002, 532(1-2), 231-236.
[http://dx.doi.org/10.1016/S0014-5793(02)03687-6] [PMID: 12459496]
[88]
Vetriani, C.; Maeder, D.L.; Tolliday, N.; Yip, K.S.; Stillman, T.J.; Britton, K.L.; Rice, D.W.; Klump, H.H.; Robb, F.T. Protein thermostability above 100 degreesC: a key role for ionic interactions. Proc. Natl. Acad. Sci. USA, 1998, 95(21), 12300-12305.
[http://dx.doi.org/10.1073/pnas.95.21.12300] [PMID: 9770481]
[89]
Querol, E.; Perez-Pons, J.A.; Mozo-Villarias, A. Analysis of protein conformational characteristics related to thermostability. Protein Eng., 1996, 9(3), 265-271.
[http://dx.doi.org/10.1093/protein/9.3.265] [PMID: 8736493]
[90]
Thompson, M.J.; Eisenberg, D. Transproteomic evidence of a loop-deletion mechanism for enhancing protein thermostability. J. Mol. Biol., 1999, 290(2), 595-604.
[http://dx.doi.org/10.1006/jmbi.1999.2889] [PMID: 10390356]
[91]
Spector, S.; Wang, M.; Carp, S.A.; Robblee, J.; Hendsch, Z.S.; Fairman, R.; Tidor, B.; Raleigh, D.P. Rational modification of protein stability by the mutation of charged surface residues. Biochemistry, 2000, 39(5), 872-879.
[http://dx.doi.org/10.1021/bi992091m] [PMID: 10653630]
[92]
Wyss, D.F.; Choi, J.S.; Li, J.; Knoppers, M.H.; Willis, K.J.; Arulanandam, A.R.; Smolyar, A.; Reinherz, E.L.; Wagner, G. Conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science, 1995, 269(5228), 1273-1278.
[http://dx.doi.org/10.1126/science.7544493] [PMID: 7544493]
[93]
Gianazza, E.; Parravicini, C.; Primi, R.; Miller, I.; Eberini, I. In silico prediction and characterization of protein post-translational modifications. J. Proteomics, 2016, 134, 65-75.
[http://dx.doi.org/10.1016/j.jprot.2015.09.026] [PMID: 26436211]
[94]
Hurley, J.H.; Dean, A.M.; Thorsness, P.E.; Koshland, D.E. Jr.; Stroud, R.M. Regulation of isocitrate dehydrogenase by phosphorylation involves no long-range conformational change in the free enzyme. J. Biol. Chem., 1990, 265(7), 3599-3602.
[http://dx.doi.org/10.2210/pdb4icd/pdb] [PMID: 2406256]
[95]
Tholey, A.; Lindemann, A.; Kinzel, V.; Reed, J. Direct effects of phosphorylation on the preferred backbone conformation of peptides: a nuclear magnetic resonance study. Biophys. J., 1999, 76(1 Pt 1), 76-87.
[http://dx.doi.org/10.1016/S0006-3495(99)77179-1] [PMID: 9876124]
[96]
Johnson, L.N.; Lewis, R.J. Structural basis for control by phosphorylation. Chem. Rev., 2001, 101(8), 2209-2242.
[http://dx.doi.org/10.1021/cr000225s] [PMID: 11749371]
[97]
Guo, Y.T.; Li, Y.M.; Zhu, Z.T.; Zhao, Y.F. Effect of the phosphate group with different negative charges on the conformation of phosphorylated Ser/Thr-Pro motif. Int. J. Pept. Res. Ther., 2005, 11(2), 159-165.
[http://dx.doi.org/10.1007/s10989-005-4710-2]
[98]
Shen, T.; Zong, C.; Hamelberg, D.; McCammon, J.A.; Wolynes, P.G. The folding energy landscape and phosphorylation: modeling the conformational switch of the NFAT regulatory domain. FASEB J., 2005, 19(11), 1389-1395.
[http://dx.doi.org/10.1096/fj.04-3590hyp] [PMID: 16126906]
[99]
Bielska, A.A.; Zondlo, N.J. Hyperphosphorylation of tau induces local polyproline II helix. Biochemistry, 2006, 45(17), 5527-5537.
[http://dx.doi.org/10.1021/bi052662c] [PMID: 16634634]
[100]
Rezaei-Ghaleh, N.; Amininasab, M.; Kumar, S.; Walter, J.; Zweckstetter, M. Phosphorylation modifies the molecular stability of β-amyloid deposits. Nat. Commun., 2016, 7, 11359.
[http://dx.doi.org/10.1038/ncomms11359] [PMID: 27072999]
[101]
Zacarías-Lara, O.J.; Correa-Basurto, J.; Bello, M. Exploring the conformational and binding properties of unphosphorylated/phosphorylated monomeric and trimeric Bcl-2 through docking and molecular dynamics simulations. Biopolymers, 2016, 105(7), 393-413.
[http://dx.doi.org/10.1002/bip.22839] [PMID: 27016043]
[102]
Canduri, F.; Perez, P.C.; Caceres, R.A.; de Azevedo, W.F. Jr. Protein kinases as targets for antiparasitic chemotherapy drugs. Curr. Drug Targets, 2007, 8(3), 389-398.
[http://dx.doi.org/10.2174/138945007780058979] [PMID: 17348832]
[103]
Stanley, N.; Esteban-Martín, S.; De Fabritiis, G. Kinetic modulation of a disordered protein domain by phosphorylation. Nat. Commun., 2014, 5, 5272.
[http://dx.doi.org/10.1038/ncomms6272] [PMID: 25348080]
[104]
Bah, A.; Vernon, R.M.; Siddiqui, Z.; Krzeminski, M.; Muhandiram, R.; Zhao, C.; Sonenberg, N.; Kay, L.E.; Forman-Kay, J.D. Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch. Nature, 2015, 519(7541), 106-109.
[http://dx.doi.org/10.1038/nature13999] [PMID: 25533957]
[105]
Zeng, J.; Jiang, F.; Wu, Y.D. Mechanism of phosphorylation-induced folding of 4E-BP2 revealed by molecular dynamics simulations. J. Chem. Theory Comput., 2017, 13(1), 320-328.
[http://dx.doi.org/10.1021/acs.jctc.6b00848] [PMID: 28068774]
[106]
Bomblies, R.; Luitz, M.P.; Zacharias, M. Molecular dynamics analysis of 4E-BP2 protein fold stabilization induced by phosphorylation. J. Phys. Chem. B, 2017, 121(15), 3387-3393.
[http://dx.doi.org/10.1021/acs.jpcb.6b08597] [PMID: 27776412]
[107]
Gopi, S.; Rajasekaran, N.; Singh, A.; Ranu, S.; Naganathan, A.N. Energetic and topological determinants of a phosphorylation-induced disorder-to-order protein conformational switch. Phys. Chem. Chem. Phys., 2015, 17(41), 27264-27269.
[http://dx.doi.org/10.1039/C5CP04765J] [PMID: 26421497]
[108]
Metskas, L.A.; Rhoades, E. Folding upon phosphorylation: translational regulation by a disorder-to-order transition. Trends Biochem. Sci., 2015, 40(5), 243-244.
[http://dx.doi.org/10.1016/j.tibs.2015.02.007] [PMID: 25769422]
[109]
Zhou, C.Y.; Jiang, F.; Wu, Y.D. Residue-specific force field based on protein coil library. RSFF2: modification of AMBER ff99SB. J. Phys. Chem. B, 2015, 119(3), 1035-1047.
[http://dx.doi.org/10.1021/jp5064676] [PMID: 25358113]
[110]
Jiang, F.; Zhou, C.Y.; Wu, Y.D. Residue-specific force field based on the protein coil library. RSFF1: modification of OPLS-AA/L. J. Phys. Chem. B, 2014, 118(25), 6983-6998.
[http://dx.doi.org/10.1021/jp5017449] [PMID: 24815738]
[111]
Zeng, J.; Jiang, F.; Wu, Y.D. Folding simulations of an α-helical hairpin motif αtα with residue-specific force fields. J. Phys. Chem. B, 2016, 120(1), 33-41.
[http://dx.doi.org/10.1021/acs.jpcb.5b09027] [PMID: 26673753]
[112]
Zeng, J.; Duan, L.; Zhang, J.Z.H.; Mei, Y. A numerically stable restrained electrostatic potential charge fitting method. J. Comput. Chem., 2013, 34(10), 847-853.
[http://dx.doi.org/10.1002/jcc.23208] [PMID: 23281029]
[113]
Zeng, J.; Jia, X.; Zhang, J.Z.H.; Mei, Y. The F130L mutation in streptavidin reduces its binding affinity to biotin through electronic polarization effect. J. Comput. Chem., 2013, 34(31), 2677-2686.
[http://dx.doi.org/10.1002/jcc.23421] [PMID: 24000160]
[114]
Ji, C.; Mei, Y.; Zhang, J.Z.H. Developing polarized protein-specific charges for protein dynamics: MD free energy calculation of pKa shifts for Asp26/Asp20 in thioredoxin. Biophys. J., 2008, 95(3), 1080-1088.
[http://dx.doi.org/10.1529/biophysj.108.131110] [PMID: 18645195]
[115]
Drazic, A.; Myklebust, L.M.; Ree, R.; Arnesen, T. The world of protein acetylation. Biochim. Biophys. Acta, 2016, 1864(10), 1372-1401.
[http://dx.doi.org/10.1016/j.bbapap.2016.06.007] [PMID: 27296530]
[116]
Potoyan, D.A.; Papoian, G.A. Regulation of the H4 tail binding and folding landscapes via Lys-16 acetylation. Proc. Natl. Acad. Sci. USA, 2012, 109(44), 17857-17862.
[http://dx.doi.org/10.1073/pnas.1201805109] [PMID: 22988066]
[117]
Winogradoff, D.; Echeverria, I.; Potoyan, D.A.; Papoian, G.A. The acetylation landscape of the H4 histone tail: Disentangling the interplay between the specific and cumulative effects. J. Am. Chem. Soc., 2015, 137(19), 6245-6253.
[http://dx.doi.org/10.1021/jacs.5b00235] [PMID: 25905561]
[118]
Chang, L.; Takada, S. Histone acetylation dependent energy landscapes in tri-nucleosome revealed by residue-resolved molecular simulations. Sci. Rep., 2016, 6, 34441.
[http://dx.doi.org/10.1038/srep34441] [PMID: 27698366]
[119]
Howe, F.S.; Boubriak, I.; Sale, M.J.; Nair, A.; Clynes, D.; Grijzenhout, A.; Murray, S.C.; Woloszczuk, R.; Mellor, J. Lysine acetylation controls local protein conformation by influencing proline isomerization. Mol. Cell, 2014, 55(5), 733-744.
[http://dx.doi.org/10.1016/j.molcel.2014.07.004] [PMID: 25127513]
[120]
Howe, F.S.; Mellor, J. Proline cis-trans isomerization is influenced by local lysine acetylation-deacetylation. Microb. Cell, 2014, 1(11), 390-392.
[http://dx.doi.org/10.15698/mic2014.11.176] [PMID: 28357218]
[121]
Wang, X.; Moore, S.C.; Laszckzak, M.; Ausió, J. Acetylation increases the alpha-helical content of the histone tails of the nucleosome. J. Biol. Chem., 2000, 275(45), 35013-35020.
[http://dx.doi.org/10.1074/jbc.M004998200] [PMID: 10938086]
[122]
Ikebe, J.; Sakuraba, S.; Kono, H. H3 histone tail conformation within the nucleosome and the impact of K14 acetylation studied using enhanced sampling simulation. PLOS Comput. Biol., 2016, 12(3) e1004788
[http://dx.doi.org/10.1371/journal.pcbi.1004788] [PMID: 26967163]
[123]
Creyghton, M.P.; Cheng, A.W.; Welstead, G.G.; Kooistra, T.; Carey, B.W.; Steine, E.J.; Hanna, J.; Lodato, M.A.; Frampton, G.M.; Sharp, P.A.; Boyer, L.A.; Young, R.A.; Jaenisch, R. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA, 2010, 107(50), 21931-21936.
[http://dx.doi.org/10.1073/pnas.1016071107] [PMID: 21106759]
[124]
Eberharter, A.; Becker, P.B. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep., 2002, 3(3), 224-229.
[http://dx.doi.org/10.1093/embo-reports/kvf053] [PMID: 11882541]
[125]
Wyss, D.F.; Wagner, G. The structural role of sugars in glycoproteins. Curr. Opin. Biotechnol., 1996, 7(4), 409-416.
[http://dx.doi.org/10.1016/S0958-1669(96)80116-9] [PMID: 8768899]
[126]
Freeze, H.H.; Schachter, H.; Kinoshita, T. Genetic disorders of glycosylation In: Essentials of Glycobiology:; Cold Spring Harbor, NY,, 2015; pp. 569-582.
[127]
Chen, M.M.; Bartlett, A.I.; Nerenberg, P.S.; Friel, C.T.; Hackenberger, C.P.; Stultz, C.M.; Radford, S.E.; Imperiali, B. Perturbing the folding energy landscape of the bacterial immunity protein Im7 by site-specific N-linked glycosylation. Proc. Natl. Acad. Sci. USA, 2010, 107(52), 22528-22533.
[http://dx.doi.org/10.1073/pnas.1015356107] [PMID: 21148421]
[128]
Price, J.L.; Shental-Bechor, D.; Dhar, A.; Turner, M.J.; Powers, E.T.; Gruebele, M.; Levy, Y.; Kelly, J.W. Context-dependent effects of asparagine glycosylation on Pin WW folding kinetics and thermodynamics. J. Am. Chem. Soc., 2010, 132(43), 15359-15367.
[http://dx.doi.org/10.1021/ja106896t] [PMID: 20936810]
[129]
Culyba, E.K.; Price, J.L.; Hanson, S.R.; Dhar, A.; Wong, C.H.; Gruebele, M.; Powers, E.T.; Kelly, J.W. Protein native-state stabilization by placing aromatic side chains in N-glycosylated reverse turns. Science, 2011, 331(6017), 571-575.
[http://dx.doi.org/10.1126/science.1198461] [PMID: 21292975]
[130]
Shental-Bechor, D.; Levy, Y. Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc. Natl. Acad. Sci. USA, 2008, 105(24), 8256-8261.
[http://dx.doi.org/10.1073/pnas.0801340105] [PMID: 18550810]
[131]
Bosques, C.J.; Tschampel, S.M.; Woods, R.J.; Imperiali, B. Effects of glycosylation on peptide conformation: a synergistic experimental and computational study. J. Am. Chem. Soc., 2004, 126(27), 8421-8425.
[http://dx.doi.org/10.1021/ja0496266] [PMID: 15237998]
[132]
Petrescu, A.J.; Milac, A.L.; Petrescu, S.M.; Dwek, R.A.; Wormald, M.R. Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology, 2004, 14(2), 103-114.
[http://dx.doi.org/10.1093/glycob/cwh008] [PMID: 14514716]
[133]
Hanson, S.R.; Culyba, E.K.; Hsu, T.L.; Wong, C.H.; Kelly, J.W.; Powers, E.T. The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc. Natl. Acad. Sci. USA, 2009, 106(9), 3131-3136.
[http://dx.doi.org/10.1073/pnas.0810318105] [PMID: 19204290]
[134]
Jayaprakash, N.G.; Surolia, A. Role of glycosylation in nucleating protein folding and stability. Biochem. J., 2017, 474(14), 2333-2347.
[http://dx.doi.org/10.1042/BCJ20170111] [PMID: 28673927]
[135]
Lu, D.; Yang, C.; Liu, Z. How hydrophobicity and the glycosylation site of glycans affect protein folding and stability: a molecular dynamics simulation. J. Phys. Chem. B, 2012, 116(1), 390-400.
[http://dx.doi.org/10.1021/jp203926r] [PMID: 22118044]
[136]
Cheng, S.; Edwards, S.A.; Jiang, Y.; Gräter, F. Glycosylation enhances peptide hydrophobic collapse by impairing solvation. ChemPhysChem, 2010, 11(11), 2367-2374.
[http://dx.doi.org/10.1002/cphc.201000205] [PMID: 20583025]
[137]
Ellis, C.R.; Maiti, B.; Noid, W.G. Specific and nonspecific effects of glycosylation. J. Am. Chem. Soc., 2012, 134(19), 8184-8193.
[http://dx.doi.org/10.1021/ja301005f] [PMID: 22524526]
[138]
S.E.. Imperiali, B., Conformational switching by asparagine-linked glycosylation. J. Am. Chem. Soc., 1997, 119(9), 2295-2296.
[http://dx.doi.org/10.1021/ja963435o]
[139]
Wang, X.Y.; Ji, C.G.; Zhang, J.Z.H. Exploring the molecular mechanism of stabilization of the adhesion domains of human CD2 by N-glycosylation. J. Phys. Chem. B, 2012, 116(38), 11570-11577.
[http://dx.doi.org/10.1021/jp304116d] [PMID: 22946557]
[140]
Finkelstein, A.V.; Badretdin, A.J.; Galzitskaya, O.V.; Ivankov, D.N.; Bogatyreva, N.S.; Garbuzynskiy, S.O. There and back again: Two views on the protein folding puzzle. Phys. Life Rev., 2017, 21, 56-71.
[http://dx.doi.org/10.1016/j.plrev.2017.01.025] [PMID: 28190683]
[141]
Hogg, P.J. Disulfide bonds as switches for protein function. Trends Biochem. Sci., 2003, 28(4), 210-214.
[http://dx.doi.org/10.1016/S0968-0004(03)00057-4] [PMID: 12713905]
[142]
Wedemeyer, W.J.; Welker, E.; Narayan, M.; Scheraga, H.A. Disulfide bonds and protein folding. Biochemistry, 2000, 39(15), 4207-4216.
[http://dx.doi.org/10.1021/bi992922o] [PMID: 10757967]
[143]
Hendrick, J.P.; Hartl, F.U. The role of molecular chaperones in protein folding. FASEB J., 1995, 9(15), 1559-1569.
[http://dx.doi.org/10.1096/fasebj.9.15.8529835] [PMID: 8529835]
[144]
Botelho, H.M.; Koch, M.; Fritz, G.; Gomes, C.M. Metal ions modulate the folding and stability of the tumor suppressor protein S100A2. FEBS J., 2009, 276(6), 1776-1786.
[http://dx.doi.org/10.1111/j.1742-4658.2009.06912.x] [PMID: 19267779]
[145]
Bushmarina, N.A.; Blanchet, C.E.; Vernier, G.; Forge, V. Cofactor effects on the protein folding reaction: acceleration of alpha-lactalbumin refolding by metal ions. Protein Sci., 2006, 15(4), 659-671.
[http://dx.doi.org/10.1110/ps.051904206] [PMID: 16522796]

Rights & Permissions Print Cite
Article Metrics
27
1
© 2024 Bentham Science Publishers | Privacy Policy