Advertisement

Biophysical Reviews

, Volume 11, Issue 3, pp 365–375 | Cite as

A look back at the molten globule state of proteins: thermodynamic aspects

  • Eva Judy
  • Nand KishoreEmail author
Review

Abstract

Interest in protein folding intermediates lies in their significance to protein folding pathways. The molten globule (MG) state is one such intermediate lying on the kinetic (and sometimes thermodynamic) pathway between native and unfolded states. Development of our qualitative and quantitative understanding of the MG state can provide deeper insight into the folding pathways and hence potentially facilitate solution of the protein folding problem. An extensive look at literature suggests that most studies into protein MG states have been largely qualitative. Attempts to obtain quantitative insights into MG states have involved application of high-sensitivity calorimetry (differential scanning calorimetry and isothermal titration calorimetry). This review addresses the progress made in this direction by discussing the knowledge gained to date, along with the future promise of calorimetry, in providing quantitative information on the structural features of MG states. Particular attention is paid to the question of whether such states share common structural features or not. The difference in the nature of the transition from the MG state to the unfolded state, in terms of cooperativity, has also been addressed and discussed.

Keywords

Molten globule state Protein folding Isothermal titration calorimetry Differential scanning calorimetry Thermal transitions Thermodynamic signatures 

Notes

References

  1. Agashe VR, Shastry MC, Udgaonkar JB (1995) Initial hydrophobic collapse in the folding of barstar. Nature 377:754–757.  https://doi.org/10.1038/377754a0 Google Scholar
  2. Anfinsen CB, Haber E, Sela M et al (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc Natl Acad Sci U S A 47:1309–1314 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC223141/pdf/pnas00213-0003.pdf Google Scholar
  3. Arai M, Kondrashkina E, Kayatekin C et al (2007) Microsecond hydrophobic collapse in the folding of Escherichia coli dihydrofolate reductase, an α/β-type protein. J Mol Biol 368:219–229.  https://doi.org/10.1016/j.jmb.2007.01.085 Google Scholar
  4. Bai JH, Xu D, Wang HR et al (1999) Evidence for the existence of an unfolding intermediate state for aminoacylase during denaturation in guanidine solutions. Biochim Biophys Acta 1430:39–45.  https://doi.org/10.1016/S0167-4838(98)00282-9 Google Scholar
  5. Balbach J, Forge V, van Nuland NA et al (1995) Following protein folding in real time using NMR spectroscopy. Nat Struct Biol 2:865–870.  https://doi.org/10.1038/nsb1095-865 Google Scholar
  6. Baliga C, Selmke B, Worobiew I et al (2019) CcdB at pH 4 forms a partially unfolded state with a dry core. Biophys J 116:807–817.  https://doi.org/10.1016/j.bpj.2019.01.026 Google Scholar
  7. Banerjee T, Kishore N (2005) 2, 2, 2-Trifluoroethanol-induced molten globule state of concanavalin A and energetics of 8-anilinonaphthalene sulfonate binding: calorimetric and spectroscopic investigation. J Phys Chem B 109:22655–22662.  https://doi.org/10.1021/jp053757r Google Scholar
  8. Barrick D, Baldwin RL (1993) The molten globule intermediate of apomyoglobin and the process of protein folding. Protein Sci 2:869–876.  https://doi.org/10.1002/pro.5560020601 Google Scholar
  9. Bryngelson JD, Onuchic JN, Socci ND et al (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis. Prot Struct Funct Bioinform 21:167–195.  https://doi.org/10.1002/prot.340210302 Google Scholar
  10. Bychkova VE, Pain RH, Ptitsyn OB (1988) The ‘molten globule’ state is involved in the translocation of proteins across membranes? FEBS Lett 238:231–234.  https://doi.org/10.1016/0014-5793(88)80485-X Google Scholar
  11. Carra JH, Murphy EC, Privalov PL (1996) Thermodynamic effects of mutations on the denaturation of T4 lysozyme. Biophys J 71:1994–2001.  https://doi.org/10.1016/S0006-3495(96)79397-9 Google Scholar
  12. Chamani J, Moosavi-Movahedi AA, Saboury AA et al (2003) Calorimetric indication of the molten globule-like state of cytochrome c induced by n-alkyl sulfates at low concentrations. J Chem Thermodyn 35:199–207.  https://doi.org/10.1016/S0021-9614(02)00312-9 Google Scholar
  13. Chiti F, Webster P, Taddei N et al (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci 96:3590–3594.  https://doi.org/10.1073/pnas.96.7.3590 Google Scholar
  14. Dijkstra MJJ, Fokkink WJ, Heringa J et al (2018) The characteristics of molten globule states and folding pathways strongly depend on the sequence of a protein. Mol Phys 116:3173–3180.  https://doi.org/10.1080/00268976.2018.1496290 Google Scholar
  15. Dill KA (1985) Theory for the folding and stability of globular proteins. Biochem 24:1501–1509.  https://doi.org/10.1021/bi00327a032 Google Scholar
  16. Dill KA, MacCallum JL (2012) The protein-folding problem, 50 years on. Science 338:1042–1046.  https://doi.org/10.1126/science.1219021 Google Scholar
  17. Dill KA, Fiebig KM, Chan HS (1993) Cooperativity in protein-folding kinetics. Proc Natl Acad Sci 90:1942–1946 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC45996/ Google Scholar
  18. Dolgikh DA, Abaturov LV, Bolotina IA et al (1985) Compact state of a protein molecule with pronounced small-scale mobility: bovine α-lactalbumin. Eur Biophys J 13:109–121.  https://doi.org/10.1007/BF00256531 Google Scholar
  19. Ferrer M, Barany G, Woodward C (1995) Partially folded, molten globule and molten coil states of bovine pancreatic trypsin inhibitor. Nat Struct Biol 2:211–217.  https://doi.org/10.1038/nsb0395-211 Google Scholar
  20. Fersht AR (1997) Nucleation mechanisms in protein folding. Curr Opin Struct Biol 7:3–9.  https://doi.org/10.1016/S0959-440X(97)80002-4 Google Scholar
  21. Fink AL, Oberg KA, Seshadri S (1998) Discrete intermediates versus molten globule models for protein folding: characterization of partially folded intermediates of apomyoglobin. Fold Des 3:19–25.  https://doi.org/10.1016/S1359-0278(98)00005-4 Google Scholar
  22. Fisher A, Taniuchi H (1992) A study of core domains, and the core domain-domain interaction of cytochrome c fragment complex. Arch Biochem Biophys 296:1–16.  https://doi.org/10.1016/0003-9861(92)90538-8 Google Scholar
  23. Forge V, Wijesinha RT, Balbach J et al (1999) Rapid collapse and slow structural reorganisation during the refolding of bovine α-lactalbumin. J Mol Biol 288:673–688.  https://doi.org/10.1006/jmbi.1999.2687 Google Scholar
  24. Go N (1984) The consistency principle in protein-structure and pathways of folding. Adv Biophys 18:149–164Google Scholar
  25. Goto Y, Calciano LJ, Fink AL (1990) Acid-induced folding of proteins. Proc Natl Acad Sci 87:573–577.  https://doi.org/10.1073/pnas.87.2.573 Google Scholar
  26. Griko YV, Privalov PL (1994) Thermodynamic puzzle of apomyoglobin unfolding. J Mol Biol 235:1318–1325.  https://doi.org/10.1006/jmbi.1994.1085 Google Scholar
  27. Gussakovsky EE, Haas E (1995) Two steps in the transition between the native and acid states of bovine α-lactalbumin detected by circular polarization of luminescence: evidence for a premolten globule state? Prot Sci 4:2319–2326.  https://doi.org/10.1002/pro.5560041109 Google Scholar
  28. Haas E (2005) The study of protein folding and dynamics by determination of intramolecular distance distributions and their fluctuations using ensemble and single-molecule FRET measurements. Chem Phys Chem 6:858–870.  https://doi.org/10.1002/cphc.200400617 Google Scholar
  29. Haas E (2012) Ensemble FRET methods in studies of intrinsically disordered proteins. In: Uversky V, Dunker A (eds) Intrinsically disordered protein analysis. Methods in molecular biology (methods and protocols), vol 895. Humana Press, Totowa, NJGoogle Scholar
  30. Haber E, Anfinsen CB (1962) Side-chain interactions governing the pairing of half-cystine residues in ribonuclease. J Biol Chem 237:1839–1844Google Scholar
  31. Hamada D, Kidokoro S, Fukada H et al (1994) Salt-induced formation of the molten globule state of cytochrome c studied by isothermal titration calorimetry. Proc Natl Acad Sci 91:10325–10329.  https://doi.org/10.1073/pnas.91.22.10325 Google Scholar
  32. Hamada D, Fukada H, Takahashi K et al (1995) Salt-induced formation of the molten globule state of apomyoglobin studied by isothermal titration calorimetry. Thermochim Acta 266:385–400.  https://doi.org/10.1016/0040-6031(95)02444-1 Google Scholar
  33. Hammarströ P, Persson M, Freskgård P-O, Mårtensson L-G, Andersson D, Jonsson B-H, Carlsson U (1999) Structural mapping of an aggregation nucleation site in a molten globule intermediate. J Biol Chem 27:32897–32903.  https://doi.org/10.1074/jbc.274.46.32897 Google Scholar
  34. Hawe A, Sutter M, Jiskoot W (2008) Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 25:1487–1499.  https://doi.org/10.1007/s11095-007-9516-9 Google Scholar
  35. Haynie DT, Freire E (1993) Structural energetics of the molten globule state. Prot Struct Funct Bioinform 16:115–140.  https://doi.org/10.1002/prot.340160202 Google Scholar
  36. Honda RP, Yamaguchi KI, Kuwata K (2014) Acid-induced molten globule state of a prion protein crucial role of strand 1-helix 1-strand 2 segment. J Biol Chem 289:30355–30363.  https://doi.org/10.1074/jbc.M114.559450 Google Scholar
  37. Iglesias MM, Elola MT, Martinez V et al (2003) Identification of an equilibrium intermediate in the unfolding process of galectin-1, which retains its carbohydrate-binding specificity. Biochim Biophys Acta Proteins Proteomics 1648:164–173.  https://doi.org/10.1016/S1570-9639(03)00119-5 Google Scholar
  38. Ithychanda SS, Dou K, Robertson SP et al (2017) Structural and thermodynamic basis of a frontometaphyseal dysplasia mutation in filamin A. J Biol Chem 292:8390–8400.  https://doi.org/10.1074/jbc.M117.776740 Google Scholar
  39. Jain R, Sharma D, Kumar R et al (2018) Structural, kinetic and thermodynamic characterizations of SDS-induced molten globule state of a highly negatively charged cytochrome c. J Biochem 165:125–137.  https://doi.org/10.1093/jb/mvy087 Google Scholar
  40. Jeng MF, Englander SW (1991) Stable submolecular folding units in a non-compact form of cytochrome c. J Mol Biol 221:1045–1061.  https://doi.org/10.1016/0022-2836(91)80191-V Google Scholar
  41. Jennings PA, Wright PE (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Sci 262:892–896.  https://doi.org/10.1126/science.8235610 Google Scholar
  42. Karplus M, Weaver DL (1976) Protein-folding dynamics. Nature 260:404–406.  https://doi.org/10.1038/260404a0 Google Scholar
  43. Kelly JW (1998) The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr Opin Struct Biol 8:101–106.  https://doi.org/10.1016/S0959-440X(98)80016-X Google Scholar
  44. Khan MKA, Rahaman H, Ahmad F (2011) Conformation and thermodynamic stability of pre-molten and molten globule states of mammalian cytochromes-c. Metallomics 3(4):327–338.  https://doi.org/10.1039/C0MT00078G Google Scholar
  45. Kim PS, Baldwin RL (1982) Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu Rev Biochem 51:459–489.  https://doi.org/10.1146/annurev.bi.51.070182.002331 Google Scholar
  46. Koshiba T, Yao M, Kobashigawa Y et al (2000) Structure and thermodynamics of the extraordinarily stable molten globule state of canine milk lysozyme. Biochem 39:3248–3257.  https://doi.org/10.1021/bi991525a Google Scholar
  47. Koshiba T, Kobashigawa Y, Demura M et al (2001) Energetics of three-state unfolding of a protein: canine milk lysozyme. Protein Eng 14:967–974.  https://doi.org/10.1093/protein/14.12.967 Google Scholar
  48. Kozak JJ, Gray HB, Wittung-Stafshede P (2018) Geometrical description of protein structural motifs. J Phys Chem B 122:11289–11294.  https://doi.org/10.1021/acs.jpcb.8b07130 Google Scholar
  49. Kulkarni P, Uversky VN (2018) Intrinsically disordered proteins and the Janus challenge. Biomol 8:179.  https://doi.org/10.3390/biom8040179 Google Scholar
  50. Kuroda Y, Kidokoro SI, Wada A (1992) Thermodynamic characterization of cytochrome c at low pH: observation of the molten globule state and of the cold denaturation process. J Mol Biol 223:1139–1153.  https://doi.org/10.1016/0022-2836(92)90265-L Google Scholar
  51. Kuwajima K (1989) The molten globule state as a clue for understanding the folding and cooperativity of globular protein structure. Prot Struct Funct Bioinformatics 6:87–103.  https://doi.org/10.1002/prot.340060202 Google Scholar
  52. Ladbury JE, Doyle ML (eds) (2004) Biocalorimetry 2: applications of calorimetry in the biological sciences. John Wiley & SonsGoogle Scholar
  53. Martin J, Langer T, Boteva R et al (1991) Chaperonin-mediated protein folding at the surface of groEL through a ‘molten globule’-like intermediate. Nat 352:36–42.  https://doi.org/10.1038/352036a0 Google Scholar
  54. Mazurenko S, Kunka A, Beerens K et al (2017) Exploration of protein unfolding by modelling calorimetry data from reheating. Sci Rep 7:16321.  https://doi.org/10.1038/s41598-017-16360-y Google Scholar
  55. Misra PP, Kishore N (2011) Biophysical analysis of partially folded state of a-lactalbumin in the presence of cationic and anionic surfactants. J Colloid Interface Sci 354:234–247.  https://doi.org/10.1016/j.jcis.2010.10.015 Google Scholar
  56. Moosavi-Movahedi AA, Chamani J, Gharanfoli M et al (2004) Differential scanning calorimetric study of the molten globule state of cytochrome c induced by sodium n-dodecyl sulfate. Thermochim Acta 409:137–144.  https://doi.org/10.1016/S0040-6031(03)00358-7 Google Scholar
  57. Munoz V, Thompson PA, Hofrichter J et al (1997) Folding dynamics and mechanism of β-hairpin formation. Nat 390:196–199.  https://doi.org/10.1038/36626 Google Scholar
  58. Nakamura S, Kidokoro SI (2012) Volumetric properties of the molten globule state of cytochrome c in the thermal three-state transition evaluated by pressure perturbation calorimetry. J Phys Chem B 116:1927–1932.  https://doi.org/10.1021/jp209686e Google Scholar
  59. Nakamura S, Baba T, Kidokoro SI (2007) A molten globule-like intermediate state detected in the thermal transition of cytochrome c under low salt concentration. Biophys Chem 127:103–112.  https://doi.org/10.1016/j.bpc.2007.01.002 Google Scholar
  60. Nakamura S, Seki Y, Katoh E et al (2011) Thermodynamic and structural properties of the acid molten globule state of horse cytochrome c. Biochem 50:3116–3126.  https://doi.org/10.1021/bi101806b Google Scholar
  61. Nishii I, Kataoka M, Goto Y (1995) Thermodynamic stability of the molten globule states of apomyoglobin. J Mol Biol 250:223–238.  https://doi.org/10.1006/jmbi.1995.0373 Google Scholar
  62. Nölting B, Agard DA (2008) How general is the nucleation–condensation mechanism? Prot Struct Funct Bioinform 73:754–764.  https://doi.org/10.1002/prot.22099 Google Scholar
  63. Ohgushi M, Wada A (1983) Molten-globule state: a compact form of globular proteins with mobile side-chains. FEBS Lett 28:21–24.  https://doi.org/10.1016/0014-5793(83)80010-6 Google Scholar
  64. Onuchic JN, Socci ND, Luthey-Schulten Z et al (1996) Protein folding funnels: the nature of the transition state ensemble. Fold Des 1:441–450.  https://doi.org/10.1016/S1359-0278(96)00060-0 Google Scholar
  65. Onuchic JN, Luthey-Schulten Z, Wolynes PG (1997) Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 48:545–600.  https://doi.org/10.1146/annurev.physchem.48.1.545 Google Scholar
  66. Paci E, Smith LJ, Dobson CM et al (2001) Exploration of partially unfolded states of human α-lactalbumin by molecular dynamics simulation. J Mol Biol 306:329–347.  https://doi.org/10.1006/jmbi.2000.4337 Google Scholar
  67. Peixoto PD, Trivelli X, André C et al (2019) Formation of β-lactoglobulin aggregates from quite, unfolded conformations upon heat activation. Langmuir 35:446–452.  https://doi.org/10.1021/acs.langmuir.8b03459 Google Scholar
  68. Penkett CJ, Redfield C, Jones JA et al (1998) Structural and dynamical characterization of a biologically active unfolded fibronectin-binding protein from Staphylococcus a ureus. Biochem 37:17054–17067.  https://doi.org/10.1021/bi9814080 Google Scholar
  69. Perutz MF, Rossman MG, Cullis AF et al (1960) Structure of haemoglobin: a three-dimensional Fourier synthesis at 5.5-Ao. resolution, obtained by X-ray analysis. Nature 185:416–422 https://www.ncbi.nlm.nih.gov/pubmed/18990801 Google Scholar
  70. Potekhin S, Pfeil W (1989) Microcalorimetric studies of conformational transitions of ferricytochrome c in acidic solution. Biophys Chem 34:55–62.  https://doi.org/10.1016/0301-4622(89)80041-9 Google Scholar
  71. Povarova OI, Kuznetsova IM, Turoverov KK (2010) Differences in the pathways of proteins unfolding induced by urea and guanidine hydrochloride: molten globule state and aggregates. PLoS One 132:e15035.  https://doi.org/10.1371/journal.pone.0015035 Google Scholar
  72. Prajapati RS, Indu S, Varadarajan R (2007) Identification and thermodynamic characterization of molten globule states of periplasmic binding proteins. Biochem 46:10339–10352.  https://doi.org/10.1021/bi700577m Google Scholar
  73. Privalov PL (1979) Stability of proteins: small globular proteins. Adv Prot Chem 33:167–241). Academic Press.  https://doi.org/10.1016/S0065-3233(08)60460-X
  74. Privalov PL, Dragan AI (2007) Microcalorimetry of biological macromolecules. Biophys Chem 126:16–24.  https://doi.org/10.1016/j.bpc.2006.05.004 Google Scholar
  75. Privalov PL, Gill SJ (1988). Stability of protein structure and hydrophobic interaction. Adv Prot Chem 39:191–234. Academic Press.  https://doi.org/10.1016/S0065-3233(08)60377-0
  76. Ptitsyn OB (1973) Stages in the mechanism of self-organization of protein molecules. Dol Akad Nauk, SSSR 210:1213–1215 https://www.ncbi.nlm.nih.gov/pubmed/4721708 Google Scholar
  77. Ptitsyn OB (1987) Protein folding: hypotheses and experiments. J Prot Chem 6:273–293.  https://doi.org/10.1007/BF00248050 Google Scholar
  78. Ptitsyn OB (1995) Molten globule and protein folding. Adv Prot Chem 47:83–229.  https://doi.org/10.1016/S0065-3233(08)60546-X Google Scholar
  79. Ptitsyn OB, Rashin AA (1975) A model of myoglobin self-organization. Biophys Chem 3:1–20.  https://doi.org/10.1016/0301-4622(75)80033-0 Google Scholar
  80. Rackovsky S, Scheraga HA (1977) Hydrophobicity, hydrophilicity, and the radial and orientational distributions of residues in native proteins. Proc Nat Acad Sci 74:5248–5251 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC431666/ Google Scholar
  81. Radibratovic M, Al-Hanish A, Minic S (2019) Stabilization of apo α-lactalbumin by binding of epigallocatechin-3-gallate: experimental and molecular dynamics study. Food Chem 278:388–395.  https://doi.org/10.1016/j.foodchem.2018.11.038 Google Scholar
  82. Rariy RV, Klibanov AM (1997) Correct protein folding in glycerol. Proc Natl Acad Sci U S A 94:13520–13523.  https://doi.org/10.1073/pnas.94.25.13520 Google Scholar
  83. Redfield C, Smith RA, Dobson CM (1994) Structural characterization of a highly–ordered ‘molten globule’ at low pH. Nat Struct Mol Biol 1:23–29.  https://doi.org/10.1038/nsb0194-23 Google Scholar
  84. Roder H, Elöve GA, Englander SW (1988) Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335:694–699.  https://doi.org/10.1038/335700a0 Google Scholar
  85. Samaddar S, Mandal AK, Mondal SK et al (2006) Solvation dynamics of a protein in the pre molten globule state. J Phys Chem B 110:21210–21215.  https://doi.org/10.1021/jp064136g Google Scholar
  86. Samanta HS, Zhuravlev PI, Hinczewski M et al (2017) Protein collapse is encoded in the folded state architecture. Soft Matt 13:3622–3638.  https://doi.org/10.1039/C7SM00074J Google Scholar
  87. Sasahara K, Demura M, Nitta K (2000) Partially unfolded equilibrium state of hen lysozyme studied by circular dichroism spectroscopy. Biochemistry 39:6475–6482.  https://doi.org/10.1021/bi992560k Google Scholar
  88. Sato S, Ward CL, Krouse ME et al (1996) Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J Biol Chem 271:635–638.  https://doi.org/10.1074/jbc.271.2.635 Google Scholar
  89. Schweiker KL, Fitz VW, Makhatadze GI (2009) Universal convergence of the specific volume changes of globular proteins upon unfolding. Biochem 48:10846–10851.  https://doi.org/10.1021/bi901220u Google Scholar
  90. Semisotnov GV, Rodionova NA, Razgulyaev OI et al (1991) Study of the “molten globule” intermediate state in protein folding by a hydrophobic fluorescent probe. Biopoly Orig Res Biomol 31:119–128.  https://doi.org/10.1002/bip.360310111 Google Scholar
  91. Shakhnovich EI, Finkelstein AV (1989) Theory of cooperative transitions in protein molecules. I. Why denaturation of globular protein is a first order phase transition. Biopoly Orig Res Biomol 28:1667–1680.  https://doi.org/10.1002/bip.360281003 Google Scholar
  92. Sharma R, Kishore N (2008) Isothermal titration calorimetric and spectroscopic studies on (alcohol+ salt) induced partially folded state of α-lactalbumin and its binding with 8-anilino-1-naphthalenesulfonic acid. J Chem Thermo 40:1141–1151.  https://doi.org/10.1016/j.jct.2008.02.009 Google Scholar
  93. Sheshadri S, Lingaraju GM, Varadarajan R (1999) Denaturant mediated unfolding of both native and molten globule states of maltose binding protein are accompanied by large ΔCp’s. Protein Sci 8:1689–1695.  https://doi.org/10.1110/ps.8.8.1689 Google Scholar
  94. Singh SK, Kishore N (2006) Elucidating the binding thermodynamics of 8-anilino-1-naphthalene sulfonic acid with the A-state of α-lactalbumin: an isothermal titration calorimetric investigation. Biopoly Orig Res Biomol 83:205–212.  https://doi.org/10.1002/bip.20547 Google Scholar
  95. Skora L, Becker S, Zweckstetter M (2010) Molten globule precursor states are conformationally correlated to amyloid fibrils of human beta-2-microglobulin. J Am Chem Soc 132:9223–9225.  https://doi.org/10.1021/ja100453e Google Scholar
  96. Stryer L (1965) The interaction of a naphthalene dye with apomyoglobin and apohemoglobin: a fluorescent probe of non-polar binding sites. J Mol Biol 13:482–495.  https://doi.org/10.1016/S0022-2836(65)80111-5 Google Scholar
  97. Svensson M, Sabharwal H, Håkansson A et al (1999) Molecular characterization of α–lactalbumin folding variants that induce apoptosis in tumor cells. J Biol Chem 274:6388–6396.  https://doi.org/10.1074/jbc.274.10.6388 Google Scholar
  98. Swaminathan R, Periasamy N, Udgaonkar JB et al (1994) Molten globule-like conformation of barstar: a study by fluorescence dynamics. J Phys Chem 98:9270–9278.  https://doi.org/10.1021/j100088a030 Google Scholar
  99. Takahashi S, Yoshida A, Oikawa H (2018) Hypothesis: structural heterogeneity of the unfolded proteins originating from the coupling of the local clusters and the long-range distance distribution. Biophys Rev 10:363–373.  https://doi.org/10.1007/s12551-018-0405-8 Google Scholar
  100. Talele P, Kishore N (2015) Thermodynamic analysis of partially folded states of myoglobin in presence of 2, 2, 2-trifluoroethanol. J Chem Thermo 84:50–59.  https://doi.org/10.1016/j.jct.2014.12.019 Google Scholar
  101. Tyagi M, Bornot A, Offmann B, de Brevern AG (2009) Analysis of loop boundaries using different local structure assignment methods. Protein Sci 18:1869–1881.  https://doi.org/10.1002/pro.198 Google Scholar
  102. Udgaonkar JB, Baldwin RL (1988) NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335 (6192):694-699Google Scholar
  103. Uversky VN (2018) Bringing darkness to light: intrinsic disorder as a means to dig into the dark proteome. Proteomics 18:1800352.  https://doi.org/10.1002/pmic.201800352 Google Scholar
  104. Uversky VN, Karnoup AS, Segel DJ et al (1998) Anion-induced folding of staphylococcal nuclease: characterization of multiple equilibrium partially folded intermediates. J Mol Biol 278:879–894.  https://doi.org/10.1006/jmbi.1998.1741 Google Scholar
  105. Van der Goot FG, Gonzalez-Manas JM, Lakey JH et al (1991) A molten-globule membrane-insertion intermediate of the pore-forming domain of colicin A. Nat 354:408–410.  https://doi.org/10.1038/354408a0 Google Scholar
  106. Vassilenko KS, Uversky VN (2002) Native-like secondary structure of molten globules. Biochim Biophys Acta Prot Struct Mol Enzy 1594:168–177.  https://doi.org/10.1016/S0167-4838(01)00303-X Google Scholar
  107. Velicelebi G, Sturtevant JM (1979) Thermodynamics of the denaturation of lysozyme in alcohol-water mixtures. Biochem 18:1180–1186.  https://doi.org/10.1021/bi00574a010 Google Scholar
  108. Wirtz H, Schafer S, Hoberg C et al (2018) Hydrophobic collapse of ubiquitin generates rapid protein–water motions. Biochem 57:3650–3657.  https://doi.org/10.1021/acs.biochem.8b00235 Google Scholar
  109. Wolynes PG, Onuchic JN, Thirumalai D (1995) Navigating the folding routes. Sci 267:1619–1619.  https://doi.org/10.1126/science.7886447 Google Scholar
  110. Xie D, Bhakuni V, Freire E (1991) Calorimetric determination of the energetics of the molten globule intermediate in protein folding: apo-.alpha.-lactalbumin. Biochem 30:10673–10678.  https://doi.org/10.1021/bi00108a010 Google Scholar
  111. Xie D, Bhakuni V, Freire E (1993) Are the molten globule and the unfolded states of apo-α-lactalbumin enthalpically equivalent? J Mol Biol 232:5–8.  https://doi.org/10.1006/jmbi.1993.1364 Google Scholar
  112. Xie Q, Guo T, Wang T et al (2003) Aspartate-induced aminoacylase folding and forming of molten globule. Int J Biochem Cell Biol 35:1558–1572.  https://doi.org/10.1016/S1357-2725(03)00131-6 Google Scholar
  113. Yutani K, Ogasahara K, Kuwajima K (1992) Absence of the thermal transition in apo-α-lactalbumin in the molten globule state: a study by differential scanning microcalorimetry. J Mol Biol 228:347–350.  https://doi.org/10.1016/0022-2836(92)90824-4 Google Scholar
  114. Zhang JS, Yang LQ, Du BR et al (2017) Higher RABEX-5 mRNA predicts unfavourable survival in patients with colorectal cancer. Eur Rev Med Pharma Sci 21:2372–2376 https://www.europeanreview.org/article/12807 Google Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of ChemistryIndian Institute of Technology BombayMumbaiIndia

Personalised recommendations