Skip to main content
SpringerLink
Log in
Book cover

High Pressure Bioscience pp 41–58Cite as

Driving Forces in Pressure-Induced Protein Transitions

  • Chapter

Part of the book series: Subcellular Biochemistry ((SCBI,volume 72))

Abstract

The molecular mechanisms underlying pressure-induced protein denaturation can be analyzed based on the pressure-dependent differences in the apparent volume occupied by amino acids inside the protein and when exposed to water in an unfolded conformation. This chapter presents a volumetric analysis of the peptide group and the 20 naturally occurring amino acid side chains in the interior of the native state, the micelle-like interior of the pressure-induced denatured state, and in the unfolded conformation modeled by low-molecular analogs of proteins. The transfer of a peptide group from the protein interior to water becomes increasingly favorable as pressure increases. This observation classifies solvation of peptide groups as a major driving force in pressure-induced protein denaturation. Polar side chains do not appear to exhibit significant pressure-dependent changes in their preference for the protein interior or solvent. The transfer of nonpolar side chains from the protein interior to water becomes more unfavorable as pressure increases. An inference can be drawn that a sizeable population of nonpolar side chains remains buried inside a solvent-inaccessible core of the pressure-induced denatured state. At elevated pressures this core, owing to the absence of structural constraints, may become packed almost as tightly as the interior of the native state. The presence and partial disappearance of large intraglobular voids is another driving force facilitating pressure-induced protein denaturation. Volumetric data presented here have implications for the kinetics of protein folding and shed light on the nature of the folding transition state ensembles.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Akasaka K, Tezuka T, Yamada H (1997) Pressure-induced changes in the folded structure of lysozyme. J Mol Biol 271:671–678

    Article  CAS  PubMed  Google Scholar 

  • Akasaka K, Li H, Yamada H, Li RH, Thoresen T, Woodward CK (1999) Pressure response of protein backbone structure. Pressure-induced amide N-15 chemical shifts in BPTI. Protein Sci 8:1946–1953

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baden N, Kajimoto O, Hara K (2002) High-pressure studies on aggregation number of surfactant micelles using the fluorescence quenching method. J Phys Chem B 106:8621–8624

    Article  CAS  Google Scholar 

  • Ben-Naim A (2012) Theoretical aspects of pressure and solute denaturation of proteins: a Kirkwood-buff-theory approach. J Chem Phys 137:235102

    Article  PubMed  Google Scholar 

  • Blandamer MJ, Davis MI, Douheret G, Reis JCR (2001) Apparent molar isentropic compressions and expansions of solutions. Chem Soc Rev 30:8–15

    Article  CAS  Google Scholar 

  • Brun TS, Hoiland H, Vikingstad E (1978) Partial molal volumes and isentropic partial molal compressibilities of surface active agents in aqueous solution. J Colloid Interface Sci 63:89–96

    Article  CAS  Google Scholar 

  • Brun L, Isom DG, Velu P, Garcia-Moreno B, Royer CA (2006) Hydration of the folding transition state ensemble of a protein. Biochemistry 45:3473–3480

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chalikian TV (2003) Volumetric properties of proteins. Annu Rev Biophys Biomol Struct 32:207–235

    Article  CAS  PubMed  Google Scholar 

  • Chalikian TV, Breslauer KJ (1996) On volume changes accompanying conformational transitions of biopolymers. Biopolymers 39:619–626

    Article  CAS  PubMed  Google Scholar 

  • Chalikian TV, Filfil R (2003) How large are the volume changes accompanying protein transitions and binding? Biophys Chem 104:489–499

    Article  CAS  PubMed  Google Scholar 

  • Chalikian TV, Macgregor RB Jr (2009) Origins of pressure-induced protein transitions. J Mol Biol 394:834–842

    Article  CAS  PubMed  Google Scholar 

  • Chalikian TV, Kharakoz DP, Sarvazyan AP, Cain CA, Mcgough RJ, Pogosova IV, Gareginian TN (1992) Ultrasonic study of proton transfer reactions in aqueous solutions of amino acids. J Phys Chem 96:876–883

    Article  Google Scholar 

  • Chalikian TV, Sarvazyan AP, Breslauer KJ (1993) Partial molar volumes, expansibilities, and compressibilities of α, ω-aminocarboxylic acids in aqueous solutions between 18 and 55°C. J Phys Chem 97:13017–13026

    Article  CAS  Google Scholar 

  • Chalikian TV, Sarvazyan AP, Funck T, Breslauer KJ (1994a) Partial molar volumes, expansibilities, and compressibilities of oligoglycines in aqueous solutions at 18–55°C. Biopolymers 34:541–553

    Article  CAS  Google Scholar 

  • Chalikian TV, Sarvazyan AP, Funck T, Cain CA, Breslauer KJ (1994b) Partial molar characteristics of glycine and alanine in aqueous solutions at high pressures calculated from ultrasonic velocity data. J Phys Chem 98:321–328

    Article  CAS  Google Scholar 

  • Chalikian TV, Gindikin VS, Breslauer KJ (1998) Hydration of diglycyl tripeptides with nonpolar side chains: a volumetric study. Biophys Chem 75:57–71

    Article  CAS  PubMed  Google Scholar 

  • Cheung MS, Garcia AE, Onuchic JN (2002) Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc Natl Acad Sci U S A 99:685–690

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Desai G, Panick G, Zein M, Winter R, Royer CA (1999) Pressure-jump studies of the folding unfolding of trp repressor. J Mol Biol 288:461–475

    Article  CAS  PubMed  Google Scholar 

  • Desnoyers JE, Philip PR (1972) Isothermal compressibilities of aqueous solutions of tetraalkylammonium bromides. Can J Chem 50:1094–1096

    Article  CAS  Google Scholar 

  • Dill KA (1990) Dominant forces in protein folding. Biochemistry 29:7133–7155

    Article  CAS  PubMed  Google Scholar 

  • Dill KA, MacCallum JL (2012) The protein-folding problem, 50 years on. Science 338:1042–1046

    Article  CAS  PubMed  Google Scholar 

  • Dill KA, Ozkan SB, Shell MS, Weikl TR (2008) The protein folding problem. Annu Rev Biophys 37:289–316

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandez-Escamilla AM, Cheung MS, Vega MC, Wilmanns M, Onuchic JN, Serrano L (2004) Solvation in protein folding analysis: combination of theoretical and experimental approaches. Proc Natl Acad Sci U S A 101:2834–2839

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gekko K, Hasegawa Y (1986) Compressibility-structure relationship of globular proteins. Biochemistry 25:6563–6571

    Article  CAS  PubMed  Google Scholar 

  • Gerstein M, Chothia C (1996) Packing at the protein-water interface. Proc Natl Acad Sci U S A 93:10167–10172

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gerstein M, Sonnhammer ELL, Chothia C (1994) Volume changes in protein evolution. J Mol Biol 236:1067–1078

    Article  CAS  PubMed  Google Scholar 

  • Gerstein M, Tsai J, Levitt M (1995) The volume of atoms on the protein surface calculated from simulation, using Voronoi polyhedral. J Mol Biol 249:955–966

    Article  CAS  PubMed  Google Scholar 

  • Ghosh T, Garcia AE, Garde S (2001) Molecular dynamics simulations of pressure effects on hydrophobic interactions. J Am Chem Soc 123:10997–11003

    Article  CAS  PubMed  Google Scholar 

  • Gucker FT, Lamb FW, Marsh GA, Haag RM (1950) The adiabatic compressibility of aqueous solutions of some simple amino acids and their uncharged isomers at 25°C. J Am Chem Soc 72:310–317

    Article  CAS  Google Scholar 

  • Hakin AW, Hoiland H, Hedwig GR (2000) Volumetric properties of some oligopeptides in aqueous solution: partial molar expansibilities and isothermal compressibilities at 298.15 K for the peptides of sequence Ala(gly)(n), n = 1–4. Phys Chem Chem Phys 2:4850–4857

    Article  CAS  Google Scholar 

  • Hara K, Suzuki H, Takisawa N (1989) High-pressure studies of a fluorescence probe for the critical micelle concentration in sodium dodecyl sulfate. J Phys Chem 93:3710–3713

    Article  CAS  Google Scholar 

  • Harpaz Y, Gerstein M, Chothia C (1994) Volume changes on protein-folding. Structure 2:641–649

    Article  CAS  PubMed  Google Scholar 

  • Hedwig GR (2006) Isentropic and isothermal compressibilities of the backbone glycyl group of proteins in aqueous solution. Biophys Chem 124:35–42

    Article  CAS  PubMed  Google Scholar 

  • Hedwig GR, Hogseth E, Hoiland H (2008) Volumetric properties of the glycyl group of proteins in aqueous solution at high pressures. Phys Chem Chem Phys 10:884–897

    Article  CAS  PubMed  Google Scholar 

  • Hummer G, Garde S, Garcia AE, Paulaitis ME, Pratt LR (1998) The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. Proc Natl Acad Sci U S A 95:1552–1555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hummer G, Garde S, Garcia AE, Pratt LR (2000) New perspectives on hydrophobic effects. Chem Phys 258:349–370

    Article  CAS  Google Scholar 

  • Imamura H, Kato M (2009) Effect of pressure on helix-coil transition of an alanine-based peptide: an FTIR study. Proteins 75:911–918

    Article  CAS  PubMed  Google Scholar 

  • Kajander T, Kahn PC, Passila SH, Cohen DC, Lehtio L, Adolfsen W, Warwicker J, Schell U, Goldman A (2000) Buried charged surface in proteins. Structure 8:1203–1214

    Article  CAS  PubMed  Google Scholar 

  • Kamatari YO, Yamada H, Akasaka K, Jones JA, Dobson CM, Smith LJ (2001) Response of native and denatured hen lysozyme to high pressure studied by 15N/1H NMR spectroscopy. Eur J Biochem 268:1782–1793

    Article  CAS  PubMed  Google Scholar 

  • Kaneshina S, Tanaka M, Tomida T, Matuura R (1974) Micelle formation of sodium alkylsulfate under high pressures. J Colloid Interface Sci 48:450–460

    Article  CAS  Google Scholar 

  • Katrusiak A, Dauter Z (1996) Compressibility of lysozyme protein crystals by X-ray diffraction. Acta Cryst Sect D 52:607–608

    Article  CAS  Google Scholar 

  • Kharakoz DP (1989) Volumetric properties of proteins and their analogs in diluted water solutions. 1. Partial volumes of amino acids at 15–55°C. Biophys Chem 34:115–125

    Article  CAS  PubMed  Google Scholar 

  • Kharakoz DP (1991) Volumetric properties of proteins and their analogs in diluted water solutions. 2. Partial adiabatic compressibilities of amino acids at 15–70°C. J Phys Chem 95:5634–5642

    Article  CAS  Google Scholar 

  • Kharakoz DP (1997) Partial volumes and compressibilities of extended polypeptide chains in aqueous solution: additivity scheme and implication of protein unfolding at normal and high pressure. Biochemistry 36:10276–10285

    Article  CAS  PubMed  Google Scholar 

  • Kharakoz DP (2000) Protein compressibility, dynamics, and pressure. Biophys J 79:511–525

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kitahara R, Yamada H, Akasaka K, Wright PE (2002) High pressure NMR reveals that apomyoglobin is an equilibrium mixture from the native to the unfolded. J Mol Biol 320:311–319

    Article  CAS  PubMed  Google Scholar 

  • Kudryashov E, Kapustina T, Morrissey S, Buckin V, Dawson K (1998) The compressibility of alkyltrimethylammonium bromide micelles. J Colloid Interface Sci 203:59–68

    Article  CAS  Google Scholar 

  • Kundrot CE, Richards FM (1987) Crystal structure of hen egg white lysozyme at a hydrostatic pressure of 1000 atmospheres. J Mol Biol 193:157–170

    Article  CAS  PubMed  Google Scholar 

  • Kundrot CE, Richards FM (1988) Effect of hydrostatic pressure on the solvent in crystals of hen egg white lysozyme. J Mol Biol 200:401–410

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Tikhomirova A, Shalvardjian N, Chalikian TV (2008) Partial molar volumes and adiabatic compressibilities of unfolded protein states. Biophys Chem 134:185–199

    Article  CAS  PubMed  Google Scholar 

  • Lesemann M, Thirumoorthy K, Kim YJ, Jonas J, Paulaitis ME (1998) Pressure dependence of the critical micelle concentration of a nonionic surfactant in water studied by H-1-NMR. Langmuir 14:5339–5341

    Article  CAS  Google Scholar 

  • Levy Y, Onuchic JN (2006) Water mediation in protein folding and molecular recognition. Annu Rev Biophys Biomol Struct 35:389–415

    Article  CAS  PubMed  Google Scholar 

  • Li H, Yamada H, Akasaka K (1998) Effect of pressure on individual hydrogen bonds in proteins, basic pancreatic trypsin inhibitor. Biochemistry 37:1167–1173

    Article  CAS  PubMed  Google Scholar 

  • Liang J, Dill KA (2001) Are proteins well-packed? Biophys J 81:751–766

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Matthews BW, Liu L (2009) A review about nothing: are apolar cavities in proteins really empty? Protein Sci 18:494–502

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moghaddam MS, Chan HS (2007) Pressure and temperature dependence of hydrophobic hydration: volumetric, compressibility, and thermodynamic signatures. J Chem Phys 126:114507

    Article  PubMed  Google Scholar 

  • Neumaier S, Buttner M, Bachmann A, Kiefhaber T (2013) Transition state and ground state properties of the helix-coil transition in peptides deduced from high-pressure studies. Proc Natl Acad Sci U S A 110:20988–20993

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Panick G, Vidugiris GJA, Malessa R, Rapp G, Winter R, Royer CA (1999) Exploring the temperature-pressure phase diagram of staphylococcal nuclease. Biochemistry 38:4157–4164

    Article  CAS  PubMed  Google Scholar 

  • Poupon A (2004) Voronoi and Voronoi-related tessellations in studies of protein structure and interaction. Curr Opin Struct Biol 14:233–241

    Article  CAS  PubMed  Google Scholar 

  • Rashin AA, Iofin M, Honig B (1986) Internal cavities and buried waters in globular proteins. Biochemistry 25:3619–3625

    Article  CAS  PubMed  Google Scholar 

  • Rasper J, Kauzmann W (1962) Volume changes in protein reactions. 1. Ionization reactions of proteins. J Am Chem Soc 84:1771–1777

    Article  CAS  Google Scholar 

  • Richards FM (1985) Calculation of molecular volumes and areas for structures of known geometry. Methods Enzymol 115:440–464

    Article  CAS  PubMed  Google Scholar 

  • Roche J, Caro JA, Norberto DR, Barthe P, Roumestand C, Schlessman JL, Garcia AE, Garcia-Moreno B, Royer CA (2012) Cavities determine the pressure unfolding of proteins. Proc Natl Acad Sci U S A 109:6945–6950

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sarvazyan AP, Chalikian TV (1989) Relationship between nonlinear acoustic properties and thermodynamic characteristics of solutions of biological substances. In Ultrasonic international 89, Butterworth, pp 704–710

    Google Scholar 

  • Shakhnovich E (2006) Protein folding thermodynamics and dynamics: where physics, chemistry, and biology meet. Chem Rev 106:1559–1588

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takekiyo T, Shimizu A, Kato M, Taniguchi Y (2005) Pressure-tuning FTIR spectroscopic study on the helix-coil transition of ala-rich oligopeptide in aqueous solution. Biochim Biophys Acta 1750:1–4

    Article  CAS  PubMed  Google Scholar 

  • Tanaka M, Kaneshina S, Tomida T, Noda K, Aoki K (1973) Effect of pressure on solubilities of ionic surfactants in water. J Colloid Interface Sci 44:525–531

    Article  CAS  Google Scholar 

  • Tanaka M, Kaneshina S, Kaoru SN, Okajima T, Tomida T (1974) Partial molal volumes of surfactant and its homologous salts under high pressure. J Colloid Interface Sci 46:132–138

    Article  CAS  Google Scholar 

  • Taulier N, Chalikian TV (2002) Compressibility of protein transitions. Biochim Biophys Acta 1595:48–70

    Article  CAS  PubMed  Google Scholar 

  • Tsai J, Gerstein M (2002) Calculations of protein volumes: sensitivity analysis and parameter database. Bioinformatics 18:985–995

    Article  CAS  PubMed  Google Scholar 

  • Tsai J, Taylor R, Chothia C, Gerstein M (1999) The packing density in proteins: standard radii and volumes. J Mol Biol 290:253–266

    Article  CAS  PubMed  Google Scholar 

  • Vidugiris GJA, Markley JL, Royer CA (1995) Evidence for a molten globule-like transition state in protein folding from determination of activation volumes. Biochemistry 34:4909–4912

    Article  CAS  PubMed  Google Scholar 

  • Winter R, Lopes D, Grudzielanek S, Vogtt K (2007) Towards an understanding of the temperature/pressure configurational and free-energy landscape of biomolecules. J Non-Equilib Thermodyn 32:41–97

    CAS  Google Scholar 

  • Woenckhaus J, Kohling R, Thiyagarajan P, Littrell KC, Seifert S, Royer CA, Winter R (2001) Pressure-jump small-angle x-ray scattering detected kinetics of staphylococcal nuclease folding. Biophys J 80:1518–1523

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Sciences, Leslie Dan Faculty of Pharmacy, University of Toronto, Toronto, ON, M5S 3 M2, Canada

    Tigran V. Chalikian

Authors
  1. Tigran V. Chalikian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tigran V. Chalikian .

Editor information

Editors and Affiliations

  1. Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Kyoto, Japan

    Kazuyuki Akasaka

  2. Department of Life System, Institute of Technology and Science, Tokushima University, Tokushima, Japan

    Hitoshi Matsuki

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Chalikian, T.V. (2015). Driving Forces in Pressure-Induced Protein Transitions. In: Akasaka, K., Matsuki, H. (eds) High Pressure Bioscience. Subcellular Biochemistry, vol 72. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9918-8_3

Download citation

Publish with us

Policies and ethics

Search

Navigation