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Research Articles

Denatured states of yeast cytochrome c induced by heat and guanidinium chloride are structurally and thermodynamically different

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Pages 1420-1435 | Received 23 Mar 2016, Accepted 28 Apr 2016, Published online: 06 Jun 2016

References

  • Ahmad, F., & Bigelow, C. C. (1979). The denaturation of ribonuclease A by combinations of urea and salt denaturants. Journal of Molecular Biology, 131, 607–617. doi:0022-2836(79)90010-X[pii]
  • Ahmad, F., & Bigelow, C. C. (1982). Estimation of the free energy of stabilization of ribonuclease A, lysozyme, alpha-lactalbumin, and myoglobin. Journal of Biological Chemistry, 257, 12935–12938.
  • Ahmad, F., Khan, M. M., Rastogi, A. K., Chaubey, M., & Kidwai, J. R. (1991). Effect of (-)epicatechin on cAMP content, insulin release and conversion of proinsulin to insulin in immature and mature rat islets in vitro. Indian Journal of Experimental Biology, 29, 516–520.
  • Ahmad, F., & Salahuddin, A. (1975). Intrinsic viscosity of ovomucoid in random coil conformation. International Journal of Peptide Protein Research, 7, 417–421.
  • Alam Khan, M. K., Das, U., Rahaman, M. H., Hassan, M. I., Srinivasan, A., Singh, T. P., & Ahmad, F. (2009). A single mutation induces molten globule formation and a drastic destabilization of wild-type cytochrome c at pH 6.0. JBIC Journal of Biological Inorganic Chemistry, 14, 751–760. doi:10.1007/s00775-009-0488-6
  • Alam Khan, M. K., Rahaman, M. H., Hassan, M. I., Singh, T. P., Moosavi-Movahedi, A. A., & Ahmad, F. (2010). Conformational and thermodynamic characterization of the premolten globule state occurring during unfolding of the molten globule state of cytochrome c. JBIC Journal of Biological Inorganic Chemistry, 15, 1319–1329. doi:10.1007/s00775-010-0691-5
  • Arcus, V. L., Vuilleumier, S., Freund, S. M., Bycroft, M., & Fersht, A. R. (1995). A Comparison of the pH, urea, and temperature-denatured states of barnase by heteronuclear NMR: Implications for the initiation of protein folding. Journal of Molecular Biology, 254, 305–321
  • Aune, K. C., Salahuddin, A., Zarlengo, M. H., & Tanford, C. (1967). Evidence for residual structure in acid- and heat-denatured proteins. Journal of Biological Chemistry, 242, 4486–4489.
  • Basharov, M. A. (2012). Residual ordered structure in denatured proteins and the problem of protein folding. Indian Journal of Biochemistry & Biophysics, 49, 7–17.
  • Berry, G. C. (2010). The hydrodynamic and conformational properties of denatured proteins in dilute solutions. Protein Science, 19, 94–98. doi:10.1002/pro.286
  • Bowler, B. E. (2012). Residual structure in unfolded proteins. Current Opinion in Structural Biology, 22, 4–13.
  • Camilloni, C., Rocco, A. G., Eberini, I., Gianazza, E., Broglia, R. A., & Tiana, G. (2008). Urea and guanidinium chloride denature protein L in different ways in molecular dynamics simulations. Biophysical Journal, 94, 4654–4661. doi:10.1529/biophysj.107.125799
  • Chalikian, T. V., Volker, J., Anafi, D., & Breslauer, K. J. (1997). The native and the heat-induced denatured states of α-chymotrypsinogen A: Thermodynamic and spectroscopic studies. Journal of Molecular Biology, 274, 237–252. doi:10.1006/jmbi.1997.1394
  • Choudhary, R. K., Vikrant, S. Q. M., Thapa, P. S., Raikundalia, S., Gadewal, N., Kumar, N. S., … Varma, A. K. (2015). Multimodal approach to explore the pathogenicity of BARD1, ARG 658 CYS, and ILE 738 VAL mutants. Journal of Biomolecular Structure and Dynamics, 1–12. doi: 10.1080/07391102.2015.1082149
  • Dalal, S., Mhashal, A., Kadoo, N., & Gaikwad, S. M. (2016). Functional stability and structural transitions of Kallikrein: Spectroscopic and molecular dynamics studies. Journal of Biomolecular Structure and Dynamics, 1–13. doi:10.1080/07391102.2016.1138884
  • Drobnak, I., Vesnaver, G., & Lah, J. (2010). Model-based thermodynamic analysis of reversible unfolding processes. The Journal of Physical Chemistry B, 114, 8713–8722. doi:10.1021/jp100525m
  • Fersht, A. R. (1997). Nucleation mechanisms in protein folding. Current Opinion in Structural Biology, 7, 3–9.
  • Fink, A. L., Calciano, L. J., Goto, Y., Kurotsu, T., & Palleros, D. R. (1994). Classification of acid denaturation of proteins: Intermediates and unfolded states. Biochemistry, 33, 12504–12511.10.1021/bi00207a018
  • Francis, C. J., Lindorff-Larsen, K., Best, R. B., & Vendruscolo, M. (2006). Characterization of the residual structure in the unfolded state of the Δ131Δ fragment of staphylococcal nuclease. Proteins: Structure, Function, and Bioinformatics, 65, 145–152. doi:10.1002/prot.21077
  • Godbole, S., Dong, A., Garbin, K., & Bowler, B. E. (1997). A lysine 73 –> histidine variant of yeast iso-1-cytochrome c: evidence for a native-like intermediate in the unfolding pathway and implications for m value effects. Biochemistry, 36, 119–126. doi:10.1021/bi961915mbi961915m[pii]
  • Goldstein, R. A. (2011). The evolution and evolutionary consequences of marginal thermostability in proteins. Proteins: Structure, Function, and Bioinformatics, 79, 1396–1407. doi:10.1002/prot.22964
  • Goto, Y., Calciano, L. J., & Fink, A. L. (1990). Acid-induced folding of proteins. Proceedings of the National Academy of Sciences, 87, 573–577.10.1073/pnas.87.2.573
  • Goto, Y., & Fink, A. L. (1994). Acid-induced folding of heme proteins. Methods in Enzymology, 232, 3–15.
  • Goto, Y., Takahashi, N., & Fink, A. L. (1990). Mechanism of acid-induced folding of proteins. Biochemistry, 29, 3480–3488.10.1021/bi00466a009
  • Greenfield, N. J. (2006). Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nature Protocols, 1, 2527–2535.
  • Hackel, M., Konno, T., & Hinz, H. (2000). A new alternative method to quantify residual structure in ‘unfolded’ proteins. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology, 1479, 155–165. doi:S0167483800000510[pii]
  • Hammack, B. N., Smith, C. R., & Bowler, B. E. (2001). Denatured state thermodynamics: Residual structure, chain stiffness and scaling factors. Journal of Molecular Biology, 311, 1091–1104. doi:10.1006/jmbi.2001.4909S0022-2836(01)94909-5[pii]
  • Haque, M. A., Ubaid-ullah, S., Zaidi, S., Hassan, M. I., Islam, A., Batra, J. K., & Ahmad, F. (2015). Characterization of pre-molten globule state of yeast iso-1-cytochrome c and its deletants at pH 6.0 and 25 degrees C. International Journal of Biological Macromolecules, 72, 1406–1418. doi:10.1016/j.ijbiomac.2014.10.053S0141-8130(14)00733-8[pii]
  • Haque, M. A., Zaidi, S., Ubaid-Ullah, S., Prakash, A., Hassan, M. I., Islam, A., … Ahmad, F. (2015). In vitro and in silico studies of urea-induced denaturation of yeast iso-1-cytochrome c and its deletants at pH 6.0 and 25 degrees C. Journal of Biomolecular Structure & Dynamics, 33, 1493–1502. doi:10.1080/07391102.2014.958760
  • Herrmann, L. M., & Bowler, B. E. (1997). Thermal denaturation of iso-1-cytochrome c variants: Comparison with solvent denaturation. Protein Science, 657–665. doi:10.1002/pro.5560060315
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: visual molecular dynamics. Journal of Molecular Graphics, 14, 27–38.
  • Ishtikhar, M., Khan, A., Chang, C. K., Lin, L. T., Wang, S. S., & Khan, R. H. (2016). Effect of guanidine hydrochloride and urea on the interaction of 6-thioguanine with human serum albumin: A spectroscopic and molecular dynamics based study. Journal of Biomolecular Structure and Dynamics, 1–12. doi:10.1080/07391102.2015.1054433
  • Juneja, J., & Udgaonkar, J. B. (2003). NMR studies of protein folding. Current Science, 84, 157–172.
  • Kohn, J. E., Millett, I. S., Jacob, J., Zagrovic, B., Dillon, T. M., Cingel, N., … Plaxco, K. W. (2004). Random-coil behavior and the dimensions of chemically unfolded proteins. Proceedings of the National Academy of Sciences, 101, 12491–12496. doi:10.1073/pnas.04036431010403643101[pii]
  • Kristinsson, R., & Bowler, B. E. (2005). Communication of stabilizing energy between substructures of a protein. Biochemistry, 44, 2349–2359. doi:10.1021/bi048141r
  • Kuwajima, K. (1989). The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins: Structure, Function, and Genetics, 6, 87–103. doi:10.1002/prot.340060202
  • Lett, C. M., Rosu-Myles, M. D., Frey, H. E., & Guillemette, J. G. (1999). Rational design of a more stable yeast iso-1-cytochrome c. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology, 1432, 40–48. doi:S0167-4838(99)00071-0[pii]
  • Liggins, J. R., Sherman, F., Mathews, A. J., & Nall, B. T. (1994). Differential scanning calorimetric study of the thermal unfolding transitions of yeast iso-1 and iso-2 cytochromes c and three composite isozymes. Biochemistry, 33, 9209–9219.10.1021/bi00197a024
  • Lindquist, S. L., & Kelly, J. W. (2011). Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Cold Spring Harbor Perspectives in Biology, 3. doi:10.1101/cshperspect.a004507
  • Linske-O’Connell, L. I., Sherman, F., & McLendon, G. (1995). Stabilizing amino acid replacements at position 52 in yeast iso-1-cytochrome c: In vivo and in vitro effects. Biochemistry, 34, 7094–7102.10.1021/bi00021a022
  • Logan, T. M., Thériault, Y., & Fesik, S. W. (1994). Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. Journal of Molecular Biology, 236, 637–648. doi:S0022-2836(84)71173-9[pii]10.1006/jmbi.1994.1173
  • Louie, G. V., & Brayer, G. D. (1990). High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c. Journal of Molecular Biology, 214, 527–555.
  • Margoliash, E., & Frohwirt, N. (1959). Spectrum of horse-heart cytochrome c. Biochemical Journal, 71, 570–572.10.1042/bj0710570
  • McCarney, E. R., Kohn, J. E., & Plaxco, K. W. (2005). Is there or isn’t there? The case for (and against) residual structure in chemically denatured proteins. Critical Reviews in Biochemistry and Molecular Biology, 40, 181–189. doi:TR41124243M055P5[pii]10.1080/10409230591008143
  • Moza, B., Qureshi, S. H., & Ahmad, F. (2003). Equilibrium studies of the effect of difference in sequence homology on the mechanism of denaturation of bovine and horse cytochromes-c. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1646, 49–56. doi:S1570963902005484[pii]
  • Moza, B., Qureshi, S. H., Islam, A., Singh, R., Anjum, F., Moosavi-Movahedi, A. A., & Ahmad, F. (2006). A unique molten globule state occurs during unfolding of cytochrome c by LiClO4 near physiological pH and temperature: structural and thermodynamic characterization. Biochemistry, 45, 4695–4702. doi:10.1021/bi052357r
  • Naiyer, A., Hassan, M. I., Islam, A., Sundd, M., & Ahmad, F. (2015). Structural characterization of MG and pre-MG states of proteins by MD simulations, NMR, and other techniques. Journal of Biomolecular Structure and Dynamics, 33, 2267–2284. doi:10.1080/07391102.2014.999354
  • Nozaki, Y. (1972). The preparation of guanidine hydrochloride. Methods in Enzymology, 26, 43–50.10.1016/S0076-6879(72)26005-0
  • Privalov, P. L. (1979). Stability of proteins: Small globular proteins. Advance in Protein Chemistry, 33, 167–241.10.1016/S0065-3233(08)60460-X
  • Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., … Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 29, 845–854. doi:10.1093/bioinformatics/btt055
  • Ptitsyn, O. B. (1995a). How the molten globule became. Trends in Biochemical Sciences, 20, 376–379. doi:S0968-0004(00)89081-7[pii]
  • Ptitsyn, O. B. (1995b). Molten globule and protein folding. Advance in Protein Chemistry, 47, 83–229.10.1016/S0065-3233(08)60546-X
  • Ptitsyn, O. B. (1995c). Structures of folding intermediates. Current Opinion in Structural Biology, 5, 74–78.10.1016/0959-440X(95)80011-O
  • Ptitsyn, O. B., Bychkova, V. E., & Uversky, V. N. (1995). Kinetic and equilibrium folding intermediates. Philosophical Transactions of the Royal Society B: Biological Sciences, 348, 35–41. doi:10.1098/rstb.1995.0043
  • Rahaman, H., Khan, K. A., Hassan, I., Wahid, M., Singh, S. B., Singh, T. P., … Ahmad, F. (2008). Sequence and stability of the goat cytochrome c. Biophysical Chemistry, 138, 23–28. doi:S0301-4622(08)00169-5[pii]10.1016/j.bpc.2008.08.008
  • Ratcliff, K., & Marqusee, S. (2010). Identification of residual structure in the unfolded state of ribonuclease H1 from the moderately thermophilic Chlorobium tepidum: comparison with thermophilic and mesophilic homologues. Biochemistry, 49, 5167–5175. doi:10.1021/bi1001097
  • Rehman, M. T., Faheem, M., & Khan, A. U. (2015). An insight into the biophysical characterization of different states of cefotaxime hydrolyzing β-lactamase 15 (CTX-M-15). Journal of Biomolecular Structure and Dynamics, 33, 625–638. doi:10.1080/07391102.2014.899925
  • Rose, G. D., Gierasch, L. M., & Smith, J. A. (1985). Turns in peptides and proteins. Advances in Protein Chemistry, 37, 1–109.10.1016/S0065-3233(08)60063-7
  • 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, 97, 8312–8317. doi:10.1073/pnas.150239397150239397[pii]
  • Santoro, M. M., & Bolen, D. W. (1988). Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry, 27, 8063–8068.10.1021/bi00421a014
  • Singh, R., Ali Dar, T., Ahmad, S., Moosavi-Movahedi, A. A., & Ahmad, F. (2008). A new method for determining the constant-pressure heat capacity change associated with the protein denaturation induced by guanidinium chloride (or urea). Biophysical Chemistry, 133, 81–89. doi:S0301-4622(07)00295-5[pii]10.1016/j.bpc.2007.12.006
  • Singh, R., Hassan, M. I., Islam, A., & Ahmad, F. (2015). Cooperative unfolding of residual structure in heat denatured proteins by urea and guanidinium chloride. PLoS One, 10, e0128740. doi:10.1371/journal.pone.0128740PONE-D-15-06397[pii]
  • Swint, L. & Robertson, A. D. (1993). Thermodynamics of unfolding for turkey ovomucoid third domain: Thermal and chemical denaturation. Protein Science, 2, 2037–2049. doi:10.1002/pro.5560021205
  • Tamura, Y., & Gekko, K. (1995). Compactness of thermally and chemically denatured ribonuclease A as revealed by volume and compressibility. Biochemistry, 34, 1878–1884.10.1021/bi00006a008
  • Taneja, S., & Ahmad, F. (1994). Increased thermal stability of proteins in the presence of amino acids. Biochemical Journal, 303, 147–153.10.1042/bj3030147
  • Tanford, C. (1968). Protein denaturation. Advances in Protein Chemistry, 23, 121–282.10.1016/S0065-3233(08)60401-5
  • Taverna, D. M., & Goldstein, R. A. (2002). Why are proteins marginally stable? Proteins: Structure, Function, and Genetics, 46, 105–109. doi:10.1002/prot.10016[pii]
  • Tiffany, M. L., & Krimm, S. (1972). Effect of temperature on the circular dichroism spectra of polypeptides in the extended state. Biopolymers, 11, 2309–2316. doi:10.1002/bip.1972.360111109
  • Tiffany, M. L., & Krimm, S. (1973). Extended conformations of polypeptides and proteins in urea and guandine hydrochloride. Biopolymers, 12, 575–587.10.1002/(ISSN)1097-0282
  • Ubaid-ullah, S., Haque, M. A., Zaidi, S., Hassan, M. I., Islam, A., Batra, J. K., … Ahmad, F. (2014). Effect of sequential deletion of extra N-terminal residues on the structure and stability of yeast iso-1-cytochrome-c. Journal of Biomolecular Structure and Dynamics, 32, 2005–2016. doi:10.1080/07391102.2013.848826
  • Wang, X., Wang, M., Tong, Y., Shan, L., & Wang, J. (2006). Probing the folding capacity and residual structures in 1–79 residues fragment of staphylococcal nuclease by biophysical and NMR methods. Biochimie, 88, 1343–1355. doi:10.1016/j.biochi.2006.05.002
  • Williams, P. D., Pollock, D. D., & Goldstein, R. A. (2006). Functionality and the evolution of marginal stability in proteins: inferences from lattice simulations. Evolutionary Bioinformatics Online, 2, 91–101.
  • Woody, R. W. (1992). Circular dichroism and conformation of unordered polypeptides. Adv Biophys Chem, 2, 27–79.
  • Yadav, S., & Ahmad, F. (2000). A New Method for the Determination of Stability Parameters of Proteins from Their Heat-Induced Denaturation Curves. Analytical Biochemistry, 283, 207–213. doi:10.1006/abio.2000.4641S0003-2697(00)94641-4[pii]
  • Yang, J. T., Wu, C. S., & Martinez, H. M. (1986). Calculation of protein conformation from circular dichroism. Methods Enzymol, 130, 208–269.10.1016/0076-6879(86)30013-2

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