145
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Polyols, increasing global stability of cytochrome c, destabilize the thermal unfolding intermediate

ORCID Icon & ORCID Icon
Pages 11216-11228 | Received 27 May 2021, Accepted 12 Jul 2021, Published online: 24 Jul 2021

References

  • Agashe, V. R., & Udgaonkar, J. B. (1995). Thermodynamics of denaturation of barstar: Evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride. Biochemistry, 34(10), 3286–3299. https://doi.org/10.1021/bi00010a019
  • Anjum, F., Rishi, V., & Ahmad, F. (2000). Compatibility of osmolytes with Gibbs energy of stabilization of proteins. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1476(1), 75–84. https://doi.org/10.1016/S0167-4838(99)00215-0
  • Anumalla, B., & Prabhu, N. P. (2018). Glutamate induced thermal equilibrium intermediate and counteracting effect on chemical denaturation of proteins. The Journal of Physical Chemistry B, 122(3), 1132–1144. https://doi.org/10.1021/acs.jpcb.7b10561
  • Apetri, A. C., & Surewicz, W. K. (2003). Atypical effect of salts on the thermodynamic stability of human prion protein. The Journal of Biological Chemistry, 278(25), 22187–22192. https://doi.org/10.1074/jbc.M302130200
  • Arakawa, T. (2018). Protein-solvent interaction. Biophysical Reviews, 10(2), 203–208. https://doi.org/10.1007/s12551-017-0339-6
  • Baldwin, R. L. (1996). On-pathway versus off-pathway folding intermediates. Folding & Design, 1(1), R1–R8. https://doi.org/10.1016/S1359-0278(96)00003-X
  • Beermann, B., Guddorf, J., Boehm, K., Albers, A., Kolkenbrock, S., Fetzner, S., & Hinz, H.-J. (2007). Stability, unfolding, and structural changes of cofactor-free 1H-3-hydroxy-4-oxoquinaldine 2,4-dioxygenase. Biochemistry, 46(14), 4241–4249. https://doi.org/10.1021/bi0622423
  • Bhuyan, A. K. (2010). The off-pathway status of the alkali molten globule is unrelated to heme misligation and trans-pH effects: Experiments with ferrocytochrome c. Biochemistry, 49(36), 7774–7782. https://doi.org/10.1021/bi100881n
  • Bhuyan, A. K., & Udgaonkar, J. B. (1999). Observation of multistate kinetics during the slow folding and unfolding of barstar. Biochemistry, 38(28), 9158–9168. https://doi.org/10.1021/bi990285w
  • Bhuyan, A. K., & Udgaonkar, J. B. (2001). Folding of horse cytochrome c in the reduced state. Journal of Molecular Biology, 312(5), 1135–1160. https://doi.org/10.1006/jmbi.2001.4993
  • Bolen, D. W., & Baskakov, I. V. (2001). The osmophobic effect: Natural selection of a thermodynamic force in protein folding11Edited by D. Draper. Journal of Molecular Biology, 310(5), 955–963. https://doi.org/10.1006/jmbi.2001.4819
  • Bongiovanni, C., Sinibaldi, F., Ferri, T., & Santucci, R. (2002). Glycerol-induced formation of the molten globule from acid-denatured cytochrome c: Implication for hierarchical folding. Journal of Protein Chemistry, 21(1), 35–41. https://doi.org/10.1023/A:1014179031881
  • Burg, M. B., & Ferraris, J. D. (2008). Intracellular organic osmolytes: Function and regulation. The Journal of Biological Chemistry, 283(12), 7309–7313. https://doi.org/10.1074/jbc.R700042200
  • Bushnell, G. W., Louie, G. V., & Brayer, G. D. (1990). High-resolution three-dimensional structure of horse heart cytochrome c. Journal of Molecular Biology, 214(2), 585–595. https://doi.org/10.1016/0022-2836(90)90200-6
  • Camilloni, C., Guerini Rocco, A., Eberini, I., Gianazza, E., Broglia, R. A., & Tiana, G. (2008). Urea and guanidinium chloride denature protein in different ways in molecular dynamics simulations. Biophysical Journal, 94(12), 4654–4661. https://doi.org/10.1529/biophysj.107.125799
  • Canchi, D. R., & García, A. E. (2013). Cosolvent effects on protein stability. Annual Review of Physical Chemistry, 64(1), 273–293. https://doi.org/10.1146/annurev-physchem-040412-110156
  • Chamberlain, A. K., & Marqusee, S. B. T.A. (2000). Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Protein folding mechanisms (Vol. 53, pp. 283–328). Academic Press. https://doi.org/10.1016/S0065-3233(00)53006-X
  • Cremades, N., & Sancho, J. (2008). Molten globule and native state ensemble of helicobacter pylori flavodoxin: Can crowding, osmolytes or cofactors stabilize the native conformation relative to the molten globule? Biophysical Journal, 95(4), 1913–1927. https://doi.org/10.1529/biophysj.108.130153
  • Das, A., & Mukhopadhyay, C. (2009). Urea-mediated protein denaturation: A consensus view. The Journal of Physical Chemistry B, 113(38), 12816–12824. https://doi.org/10.1021/jp906350s
  • Dasgupta, A., & Udgaonkar, J. B. (2012). Four-state folding of a SH3 domain: Salt-induced modulation of the stabilities of the intermediates and native state. Biochemistry, 51(23), 4723–4734. https://doi.org/10.1021/bi300223b
  • Dempsey, C. E., Piggot, T. J., & Mason, P. E. (2005). Dissecting contributions to the denaturant sensitivities of proteins. Biochemistry, 44(2), 775–781. https://doi.org/10.1021/bi048389g
  • Devaraneni, P. K., Mishra, N., & Bhat, R. (2012). Polyol osmolytes stabilize native-like cooperative intermediate state of yeast hexokinase A at low pH. Biochimie, 94(4), 947–952. https://doi.org/10.1016/j.biochi.2011.12.012
  • Ferreon, A. C. M., & Bolen, D. W. (2004). Thermodynamics of denaturant-induced unfolding of a protein that exhibits variable two-state denaturation. Biochemistry, 43(42), 13357–13369. https://doi.org/10.1021/bi048666j
  • Franks, F., & Hatley, R. H. M. (1991). Stability of proteins at subzero temperatures: Thermodynamics and some ecological consequences. Pure and Applied Chemistry, 63(10), 1367–1380. https://doi.org/10.1351/pac199163101367
  • Freire, E., & Murphy, K. P. (1991). Molecular basis of co-operativity in protein folding. Journal of Molecular Biology, 222(3), 687–698. https://doi.org/10.1016/0022-2836(91)90505-Z
  • Fujiwara, K., Arai, M., Shimizu, A., Ikeguchi, M., Kuwajima, K., & Sugai, S. (1999). Folding-unfolding equilibrium and kinetics of equine beta-lactoglobulin: Equivalence between the equilibrium molten globule state and a burst-phase folding intermediate. Biochemistry, 38(14), 4455–4463. https://doi.org/10.1021/bi982683p
  • Gekko, K. (1981). Mechanism of polyol-induced protein stabilization: Solubility of amino acids and diglycine in aqueous polyol solutions. Journal of Biochemistry, 90(6), 1633–1641. https://doi.org/10.1093/oxfordjournals.jbchem.a133638
  • Hagarman, A., Duitch, L., & Schweitzer-Stenner, R. (2008). The conformational manifold of ferricytochrome c explored by visible and far-UV electronic circular dichroism spectroscopy. Biochemistry, 47(36), 9667–9677. https://doi.org/10.1021/bi800729w
  • Haldar, S., & Chattopadhyay, K. (2012). Interconnection of salt-induced hydrophobic compaction and secondary structure formation depends on solution conditions: Revisiting early events of protein folding at single molecule resolution. The Journal of Biological Chemistry, 287(14), 11546–11555. https://doi.org/10.1074/jbc.M111.315648
  • Haldar, S., Mitra, S., & Chattopadhyay, K. (2010). Role of protein stabilizers on the conformation of the unfolded state of cytochrome and its early folding kinetics: INVESTIGATION AT SINGLE MOLECULAR RESOLUTION. Journal of Biological Chemistry, 285(33), 25314–25323. https://doi.org/10.1074/jbc.M110.116673
  • Hamada, D., Kidokoro, S., Fukada, H., Takahashi, K., & Goto, Y. (1994). Salt-induced formation of the molten globule state of cytochrome c studied by isothermal titration calorimetry. Proceedings of the National Academy of Sciences of the United States of America, 91(22), 10325– 10329. https://doi.org/10.1073/pnas.91.22.10325
  • Hannibal, L., Tomasina, F., Capdevila, D. A., Demicheli, V., Tórtora, V., Alvarez-Paggi, D., Jemmerson, R., Murgida, D. H., & Radi, R. (2016). Alternative conformations of cytochrome c: Structure, function, and detection. Biochemistry, 55(3), 407–428. https://doi.org/10.1021/acs.biochem.5b01385
  • Haque, I., Islam, A., Singh, R., Moosavi-Movahedi, A. A., & Ahmad, F. (2006). Stability of proteins in the presence of polyols estimated from their guanidinium chloride-induced transition curves at different pH values and 25 degrees C. Biophysical Chemistry, 119(3), 224–233. https://doi.org/10.1016/j.bpc.2005.09.016
  • Hasan, T., Kumari, K., Devi, S. C., Handa, J., Rehman, T., Ansari, N. A., & Singh, L. R. (2019). Osmolytes in vaccine production, flocculation and storage: A critical review. Human Vaccines & Immunotherapeutics, 15(2), 514–525. https://doi.org/10.1080/21645515.2018.1526585
  • Hoeltzli, S. D., & Frieden, C. (1995). Stopped-flow NMR spectroscopy: Real-time unfolding studies of 6-19F-tryptophan-labeled Escherichia coli dihydrofolate reductase. Proceedings of the National Academy of Sciences of the United States of America, 92(20), 9318– 9322. https://doi.org/10.1073/pnas.92.20.9318
  • Hu, W., Kan, Z. Y., Mayne, L., & Englander, S. W. (2016). Cytochrome c folds through foldon-dependent native-like intermediates in an ordered pathway. Proceedings of the National Academy of Sciences of the United States of America, 113(14), 3809– 3814. https://doi.org/10.1073/pnas.1522674113
  • Ikeguchi, M., Kuwajima, K., Mitani, M., & Sugai, S. (1986). Evidence for identity between the equilibrium unfolding intermediate and a transient folding intermediate: A comparative study of the folding reactions of alpha-lactalbumin and lysozyme. Biochemistry, 25(22), 6965–6972. https://doi.org/10.1021/bi00370a034
  • Ivarsson, Y., Travaglini-Allocatelli, C., Jemth, P., Malatesta, F., Brunori, M., & Gianni, S. (2007). An On-pathway intermediate in the folding of a PDZ domain. The Journal of Biological Chemistry, 282(12), 8568–8572. https://doi.org/10.1074/jbc.M611026200
  • Jennings, P. A., & Wright, P. E. (1993). Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science, 262(5135), 892– 896. https://doi.org/10.1126/science.8235610
  • Jha, S. K., & Udgaonkar, J. B. (2009). Direct evidence for a dry molten globule intermediate during the unfolding of a small protein. Proceedings of the National Academy of Sciences of the United States of America, 106(30), 12289–12294. https://doi.org/10.1073/pnas.0905744106
  • Jones, C. M., Henry, E. R., Hu, Y., Chan, C. K., Luck, S. D., Bhuyan, A., Roder, H., Hofrichter, J., & Eaton, W. A. (1993). Fast events in protein folding initiated by nanosecond laser photolysis. Proceedings of the National Academy of Sciences of the United States of America, 90(24), 11860– 11864. https://doi.org/10.1073/pnas.90.24.11860
  • Joshi, K., & Bhuyan, A. K. (2020). Quasi-native transition and self-diffusion of proteins in water-glycerol mixture. Biophysical Chemistry, 257, 106274. https://doi.org/10.1016/j.bpc.2019.106274
  • Judy, E., & Kishore, N. (2019). A look back at the molten globule state of proteins: Thermodynamic aspects. Biophysical Reviews, 11(3), 365–375. https://doi.org/10.1007/s12551-019-00527-0
  • Kamiyama, T., Sadahide, Y., Nogusa, Y., & Gekko, K. (1999). Polyol-induced molten globule of cytochrome c: An evidence for stabilization by hydrophobic interaction. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1434(1), 44–57. https://doi.org/10.1016/S0167-4838(99)00159-4
  • Kaushik, J. K., & Bhat, R. (1998). Thermal stability of proteins in aqueous polyol solutions: Role of the surface tension of water in the stabilizing effect of polyols. The Journal of Physical Chemistry B, 102(36), 7058–7066. https://doi.org/10.1021/jp981119l
  • Khorasanizadeh, S., Peters, I. D., & Roder, H. (1996). Evidence for a three-state model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nature Structural Biology, 3(2), 193–205. https://doi.org/10.1038/nsb0296-193
  • Khurana, R., Hate, A. T., Nath, U., & Udgaonkar, J. B. (1995). pH dependence of the stability of barstar to chemical and thermal denaturation. Protein Science, 4(6), 1133–1144. https://doi.org/10.1002/pro.5560040612
  • Kiefhaber, T., Labhardt, A. M., & Baldwin, R. L. (1995). Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature, 375(6531), 513–515. https://doi.org/10.1038/375513a0
  • Kim, Y. S., Jones, L. S., Dong, A., Kendrick, B. S., Chang, B. S., Manning, M. C., Randolph, T. W., & Carpenter, J. F. (2003). Effects of sucrose on conformational equilibria and fluctuations within the native-state ensemble of proteins. Protein Science: A Publication of the Protein Society, 12(6), 1252–1261. https://doi.org/10.1110/ps.0242603
  • Kumar, R., Prabhu, N. P., Rao, D. K., & Bhuyan, A. K. (2006). The alkali molten globule state of horse ferricytochrome c: Observation of cold denaturation. Journal of Molecular Biology, 364(3), 483–495. https://doi.org/10.1016/j.jmb.2006.09.025
  • Kumar, S., Sharma, D., & Kumar, R. (2014). Effect of urea and alkylureas on the stability and structural fluctuation of the M80-containing Ω-loop of horse cytochrome c. Biochimica et Biophysica Acta, 1844(3), 641–655. https://doi.org/10.1016/j.bbapap.2014.01.012
  • Latypov, R. F., Cheng, H., Roder, N. A., Zhang, J., & Roder, H. (2006). Structural characterization of an equilibrium unfolding intermediate in cytochrome c. Journal of Molecular Biology, 357(3), 1009–1025. https://doi.org/10.1016/j.jmb.2006.01.055
  • Liu, F. F., Ji, L., Zhang, L., Dong, X. Y., & Sun, Y. (2010). Molecular basis for polyol-induced protein stability revealed by molecular dynamics simulations. The Journal of Chemical Physics, 132(22), 225103. https://doi.org/10.1063/1.3453713
  • Makhatadze, G. I., & Privalov, P. L. (1992). Protein interactions with urea and guanidinium chloride: A calorimetric study. Journal of Molecular Biology, 226(2), 491–505. https://doi.org/10.1016/0022-2836(92)90963-K
  • Mayne, L., & Englander, S. W. (2000). Two-state vs. multistate protein unfolding studied by optical melting and hydrogen exchange. Protein Science, 9(10), 1873–1877. https://doi.org/10.1110/ps.9.10.1873
  • McClelland, L. J., Mou, T. C., Jeakins-Cooley, M. E., Sprang, S. R., & Bowler, B. E. (2014). Structure of a mitochondrial cytochrome c conformer competent for peroxidase activity. Proceedings of the National Academy of Sciences of the United States of America, 111(18), 6648– 6653. https://doi.org/10.1073/pnas.1323828111
  • Mishra, R., Bhat, R., & Seckler, R. (2007). Chemical chaperone-mediated protein folding: Stabilization of P22 tailspike folding intermediates by glycerol. Biological Chemistry, 388(8), 797–804. https://doi.org/10.1515/BC.2007.096
  • Naeem, A., & Khan, R. H. (2004). Characterization of molten globule state of cytochrome c at alkaline, native and acidic pH induced by butanol and SDS. The International Journal of Biochemistry & Cell Biology, 36(11), 2281–2292. https://doi.org/10.1016/j.biocel.2004.04.023
  • Naidu, K. T., Rao, D. K., & Prabhu, N. P. (2020). Cryo vs thermo: Duality of ethylene glycol on the stability of proteins. The Journal of Physical Chemistry B, 124(45), 10077–10088. https://doi.org/10.1021/acs.jpcb.0c06247
  • Ow, Y. L P., Green, D. R., Hao, Z., & Mak, T. W. (2008). Cytochrome c: Functions beyond respiration. Nature Reviews. Molecular Cell Biology, 9(7), 532–542. https://doi.org/10.1038/nrm2434
  • Parray, Z. A., Ahmad, F., Hassan, M. I., Hasan, I., & Islam, A. (2020). Effects of ethylene glycol on the structure and stability of myoglobin using spectroscopic, interaction, and in silico approaches: Monomer is different from those of its polymers. ACS Omega, 5(23), 13840–13850. https://doi.org/10.1021/acsomega.0c01185
  • Ptitsyn, O. B., Pain, R. H., Semisotnov, G. V., Zerovnik, E., & Razgulyaev, O. I. (1990). Evidence for a molten globule state as a general intermediate in protein folding. FEBS Letters, 262(1), 20–24. https://doi.org/10.1016/0014-5793(90)80143-7
  • Radford, S. E., Dobson, C. M., & Evans, P. A. (1992). The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature, 358(6384), 302–307. https://doi.org/10.1038/358302a0
  • Raibekas, A. A., & Massey, V. (1996). Glycerol-induced development of catalytically active conformation of Crotalus adamanteus L-amino acid oxidase in vitro. Proceedings of the National Academy of Sciences of the United States of America, 93(15), 7546– 7551. https://doi.org/10.1073/pnas.93.15.7546
  • Ramprakash, J., Doseeva, V., Galkin, A., Krajewski, W., Muthukumar, L., Pullalarevu, S., Demirkan, E., Herzberg, O., Moult, J., & Schwarz, F. P. (2008). Comparison of the chemical and thermal denaturation of proteins by a two-state transition model. Analytical Biochemistry, 374(1), 221–230. https://doi.org/10.1016/j.ab.2007.10.005
  • Raschke, T. M., & Marqusee, S. (1997). The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nature Structural Biology, 4(4), 298–304. https://doi.org/10.1038/nsb0497-298
  • Reiner, A., Henklein, P., & Kiefhaber, T. (2010). An unlocking/relocking barrier in conformational fluctuations of villin headpiece subdomain. Proceedings of the National Academy of Sciences of the United States of America, 107(11), 4955–4960. https://doi.org/10.1073/pnas.0910001107
  • Rodger, A. (2013). Far UV protein circular dichroism. In G. C. K. Roberts (Ed.), Encyclopedia of Biophysics (pp. 726–730). Springer. https://doi.org/10.1007/978-3-642-16712-6_634
  • Ruddon, R. W., & Bedows, E. (1997). Assisted protein folding. The Journal of Biological Chemistry, 272(6), 3125–3128. https://doi.org/10.1074/jbc.272.6.3125
  • Rudolph, R., & Lilie, H. (1996). In vitro folding of inclusion body proteins. The FASEB Journal, 10(1), 49–56. https://doi.org/10.1096/fasebj.10.1.8566547
  • Russell, B. S., & Bren, K. L. (2002). Denaturant dependence of equilibrium unfolding intermediates and denatured state structure of horse ferricytochrome c. Journal of Biological Inorganic Chemistry: JBIC: A Publication of the Society of Biological Inorganic Chemistry, 7(7–8), 909–916. https://doi.org/10.1007/s00775-002-0381-z
  • Russell, B. S., Melenkivitz, R., & Bren, K. L. (2000). NMR investigation of ferricytochrome c unfolding: Detection of an equilibrium unfolding intermediate and residual structure in the denatured state. Proceedings of the National Academy of Sciences of the United States of America, 97(15), 8312– 8317. https://doi.org/10.1073/pnas.150239397
  • Samuel, D., Kumar, T. K. S., Ganesh, G., Jayaraman, G., Yang, P. W., Chang, M. M., Trivedi, V. D., Wang, S. L., Hwang, K. C., Chang, D. K., & Yu, C. (2000). Proline inhibits aggregation during protein refolding. Protein Science: A Publication of the Protein Society, 9(2), 344–352. https://doi.org/10.1110/ps.9.2.344
  • Schellman, J. A. (2003). Protein stability in mixed solvents: A balance of contact interaction and excluded volume. Biophysical Journal, 85(1), 108–125. https://doi.org/10.1016/S0006-3495(03)74459-2
  • Schönfelder, J., Perez-Jimenez, R., & Muñoz, V. (2016). A simple two-state protein unfolds mechanically via multiple heterogeneous pathways at single-molecule resolution. Nature Communications, 7(1), 11777. https://doi.org/10.1038/ncomms11777
  • Sinibaldi, R., Ortore, M. G., Spinozzi, F., Carsughi, F., Frielinghaus, H., Cinelli, S., Onori, G., & Mariani, P. (2007). Preferential hydration of lysozyme in water/glycerol mixtures: A small-angle neutron scattering study. The Journal of Chemical Physics, 126(23), 235101. https://doi.org/10.1063/1.2735620
  • Smith, J. S., & Scholtz, J. M. (1996). Guanidine hydrochloride unfolding of peptide helices: Separation of denaturant and salt effects. Biochemistry, 35(22), 7292–7297. https://doi.org/10.1021/bi960341i
  • Soffer, J. B., & Schweitzer-Stenner, R. (2014). Near-exact enthalpy-entropy compensation governs the thermal unfolding of protonation states of oxidized cytochrome c. Journal of Biological Inorganic Chemistry: JBIC: A Publication of the Society of Biological Inorganic Chemistry, 19(7), 1181–1194. https://doi.org/10.1007/s00775-014-1174-x
  • Sosnick, T. R., Mayne, L., Hiller, R., & Englander, S. W. (1994). The barriers in protein folding. Nature Structural Biology, 1(3), 149–156. https://doi.org/10.1038/nsb0394-149
  • Sudrik, C. M., Cloutier, T., Mody, N., Sathish, H. A., & Trout, B. L. (2019). Understanding the role of preferential exclusion of sugars and polyols from native state IgG1 monoclonal antibodies and its effect on aggregation and reversible self-association. Pharmaceutical Research, 36(8), 109. https://doi.org/10.1007/s11095-019-2642-3
  • Taneja, S., & Ahmad, F. (1994). Increased thermal stability of proteins in the presence of amino acids. Biochemical Journal, 303(1), 147– 153. https://doi.org/10.1042/bj3030147
  • Tejaswi Naidu, K., & Prakash Prabhu, N. (2020). An able-cryoprotectant and a moderate denaturant: Distinctive character of ethylene glycol on protein stability. Journal of Biomolecular Structure and Dynamics, 1–13. https://doi.org/10.1080/07391102.2020.1819422
  • Timasheff, S. N. (1993). The control of protein stability and association by weak interactions with water: How do solvents affect these processes? Annual Review of Biophysics and Biomolecular Structure, 22(1), 67–97. https://doi.org/10.1146/annurev.bb.22.060193.000435
  • Timasheff, S. N. (1998). Control of protein stability and reactions by weakly interacting cosolvents: The simplicity of the complicated. In F. M. Richards, S. D. Eisenberg, P. S. Kim, & E. Di Cera (Ed.), Linkage thermodynamics of macromolecular interactions (Vol. 51, pp. 355–432). Academic Press. https://doi.org/10.1016/S0065-3233(08)60656-7
  • Timasheff, S. N. (2002). Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proceedings of the National Academy of Sciences of the United States of America, 99(15), 9721– 9726. https://doi.org/10.1073/pnas.122225399
  • Timasheff, S. N., & Inoue, H. (1968). Preferential binding of solvent components to proteins in mixed water-organic solvent systems. Biochemistry, 7(7), 2501–2513. https://doi.org/10.1021/bi00847a009
  • Tiwari, A., & Bhat, R. (2006). Stabilization of yeast hexokinase A by polyol osmolytes: Correlation with the physicochemical properties of aqueous solutions. Biophysical Chemistry, 124(2), 90–99. https://doi.org/10.1016/j.bpc.2006.06.003
  • Trewhella, J., Carlson, V. A. P., Curtis, E. H., & Heidorn, D. B. (1988). Differences in the solution structures of oxidized and reduced cytochrome c measured by small-angle x-ray scattering. Biochemistry, 27(4), 1121–1125. https://doi.org/10.1021/bi00404a007
  • Varhač, R., Sedláková, D., Stupák, M., & Sedlák, E. (2015). Non-two-state thermal denaturation of ferricytochrome c at neutral and slightly acidic pH values. Biophysical Chemistry, 203–204, 41–50. https://doi.org/10.1016/j.bpc.2015.05.002
  • Varhač, R., Tomášková, N., Fabián, M., & Sedlák, E. (2009). Kinetics of cyanide binding as a probe of local stability/flexibility of cytochrome c. Biophysical Chemistry, 144(1–2), 21–26. https://doi.org/10.1016/j.bpc.2009.06.001
  • Wang, W. (2000). Lyophilization and development of solid protein pharmaceuticals. International Journal of Pharmaceutics, 203(1–2), 1–60. https://doi.org/10.1016/S0378-5173(00)00423-3
  • Xu, Y., Mayne, L., & Englander, S. W. (1998). Evidence for an unfolding and refolding pathway in cytochrome c. Nature Structural Biology, 5(9), 774–778. https://doi.org/10.1038/1810
  • Yancey, P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. The Journal of Experimental Biology, 208(Pt 15), 2819– 2830. https://doi.org/10.1242/jeb.01730
  • Zhang, X., Lam, V. Q., Mou, Y., Kimura, T., Chung, J., Chandrasekar, S., Winkler, J. R., Mayo, S. L., & Shan, S. (2011). Direct visualization reveals dynamics of a transient intermediate during protein assembly. Proceedings of the National Academy of Sciences of the United States of America, 108(16), 6450– 6455. https://doi.org/10.1073/pnas.1019051108
  • Zhou, Y., Hall, C. K., & Karplus, M. (1999). The calorimetric criterion for a two-state process revisited. Protein Science: A Publication of the Protein Society, 8(5), 1064–1074. https://doi.org/10.1110/ps.8.5.1064

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.