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Physical Insights into the Bio-preservation of Proteins by Glassy Solvents: Why is Glycerol better than Trehalose at low Temperatures?

Year 2020, Volume: 8 Issue: 3, 580 - 584, 30.09.2020
https://doi.org/10.21541/apjes.637368

Abstract

Biopreservation has been a critical area of technical
and scientific research as it enables various forms biomolecular therapeutic
agents to find practical use in medicine. The mechanism at which biomimicry-inspired
solutions to stabilize biomolecules has been of a great scientific interest. We
have studied the behavior of lysozyme immersed in glycerol and trehalose, two
solvents frequently used in the bio-preservation of proteins, with the purpose
of identifying the microscopic origins of their very different dynamical
suppression capabilities. In agreement with experiments, we find that glycerol
is superior to trehalose at low temperatures, although the latter is deeper in
the glassy state, while trehalose is better at higher temperatures. We traced
the basis of this phenomenon to the different temperature dependencies of the
intermolecular hydrogen bonds between the model protein and the surrounding solvent.

References

  • [1] M. Tollinger, K. A. Crowhurst, L. E. Kay, and J. D. Forman-Kay, “Site-specific contributions to the pH dependence of protein stability,” Proc. Natl. Acad. Sci., vol. 100, no. 8, pp. 4545–4550, Apr. 2003.
  • [2] T. J. Magliery and L. Regan, “Combinatorial approaches to protein stability and structure,” Eur. J. Biochem., vol. 271, no. 9, pp. 1595–1608, May 2004.
  • [3] P. H. Yancey, “Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses,” J. Exp. Biol., vol. 208, no. 15, pp. 2819–2830, Aug. 2005.
  • [4] Mei Yang-woytowitz, Charles Yu, and Timothy Wiles, “Kits for the detection of beta-lactamases,” 8389234.
  • [5] V. R. Garigapati, D. Su, R. Khanzada, and S. J. Sawamura, “Protein stabilization formulations,” US8435943B2, 07-May-2013.
  • [6] Ali Eroglu, “Compositions and Methods for Biopreservation,” US20190098891A1, 2018.
  • [7] H. Faghihi, S. Merrikhihaghi, A. Ruholamini Najafabadi, V. Ramezani, S. Sardari, and A. Vatanara, “A Comparative Study to Evaluate the Effect of Different Carbohydrates on the Stability of Immunoglobulin G during Lyophilization and Following Storage,” Pharm. Sci., vol. 22, no. 4, pp. 251–259, Dec. 2016.
  • [8] K. Gekko and S. N. Timasheff, “Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures,” Biochemistry, vol. 20, no. 16, pp. 4667–4676, Aug. 1981.
  • [9] M. Uritani, M. Takai, and K. Yoshinaga, “Protective effect of disaccharides on restriction endonucleases during drying under vacuum1,” J. Biochem. (Tokyo), vol. 117, no. 4, pp. 774–779, Apr. 1995.
  • [10] R. B. Gregory, Ed., Protein-solvent interactions. New York, N.Y: M. Dekker, 1995.
  • [11] G. M. Sastry and N. Agmon, “Trehalose prevents myoglobin collapse and preserves its internal mobility,” Biochemistry, vol. 36, no. 23, pp. 7097–7108, Jun. 1997.
  • [12] A. Ansari et al., “Protein states and proteinquakes.,” Proc. Natl. Acad. Sci., vol. 82, no. 15, pp. 5000–5004, Aug. 1985.
  • [13] G. Caliskan et al., “Protein and solvent dynamics: How strongly are they coupled?,” J. Chem. Phys., vol. 121, no. 4, pp. 1978–1983, Jul. 2004.
  • [14] T. E. Dirama, G. A. Carri, and A. P. Sokolov, “Coupling between lysozyme and glycerol dynamics: Microscopic insights from molecular-dynamics simulations,” J. Chem. Phys., vol. 122, no. 24, p. 244910, Jun. 2005.
  • [15] T. E. Dirama, J. E. Curtis, G. A. Carri, and A. P. Sokolov, “Coupling between lysozyme and trehalose dynamics: Microscopic insights from molecular-dynamics simulations,” J. Chem. Phys., vol. 124, no. 3, p. 034901, Jan. 2006.
  • [16] David A Case, TA Darden, and J. W. Caldwell, “Amber 9,” Univ. Calif. San Franc., vol. 45, 2006.
  • [17] J. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman, and D. A. Case, “Development and testing of a general amber force field,” J. Comput. Chem., vol. 25, no. 9, pp. 1157–1174, Jul. 2004.
  • [18] “Frisch, M.J., Trucks, G.W., Schlegel, H.B., et al., (2004) Gaussian 03, revision E. 01, Gaussian Inc., Wallingford CT. - References - Scientific Research Publishing.” [Online]. Available: http://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=631962. [Accessed: 23-Jul-2019].
  • [19] M. T. Cicerone, A. Tellington, L. Trost, and A. Sokolov, “Substantially improved stability of biological agents in dried form the role of glassy dynamics in preservation of biopharmaceuticals,” Bioprocess Int., vol. 1, no. 36, pp. 36–47, 2003.
  • [20] D. A. Waller, “Protein folding,” Biochem. Educ., vol. 21, no. 1, p. 50, Jan. 1993.
  • [21] T. Ackermann, “C. L. Brooks III, M. Karplus, B. M. Pettitt. Proteins: A Theoretical Perspective of Dynamics, Structure and Thermodynamics, Volume LXXI, in: Advances in Chemical Physics, John Wiley & Sons, New York 1988. 259 Seiten, Preis: US $ 65.25,” Berichte Bunsenges. Für Phys. Chem., vol. 94, no. 1, pp. 96–96, Jan. 1990.
  • [22] R. V. Dunn, V. Réat, J. Finney, M. Ferrand, J. C. Smith, and R. M. Daniel, “Enzyme activity and dynamics: xylanase activity in the absence of fast anharmonic dynamics,” Biochem. J., vol. 346, no. 2, p. 355, Mar. 2000.
  • [23] P. W. Fenimore, H. Frauenfelder, B. H. McMahon, and R. D. Young, “Bulk-solvent and hydration-shell fluctuations, similar to - and -fluctuations in glasses, control protein motions and functions,” Proc. Natl. Acad. Sci., vol. 101, no. 40, pp. 14408–14413, Oct. 2004.
  • [24] M. T. Cicerone and C. L. Soles, “Fast dynamics and stabilization of proteins: binary glasses of trehalose and glycerol,” Biophys. J., vol. 86, no. 6, pp. 3836–3845, Jun. 2004.
  • [25] W. S. Doster and M. Settles, “The dynamical transition in proteins: the role of hydrogen bonds,” in Hydration Processes in Biology: Theoretical and Experimental Approaches, M.-C. Bellissent-Funel., vol. 305, Berlin: IOS Press, pp. 177–191.
  • [26] M. Tarek and D. J. Tobias, “Role of Protein-Water Hydrogen Bond Dynamics in the Protein Dynamical Transition,” Phys. Rev. Lett., vol. 88, no. 13, p. 138101, Mar. 2002.
  • [27] M. Mezei and D. L. Beveridge, “Theoretical studies of hydrogen bonding in liquid water and dilute aqueous solutions,” J. Chem. Phys., vol. 74, no. 1, pp. 622–632, Jan. 1981.

Proteinlerin Camsı Solventlerle Biyolojik Korunması Üzerine Fiziksel Bilgiler: Gliserol, Düşük Sıcaklıklarda Neden Trehaloz'dan Daha İyidir?

Year 2020, Volume: 8 Issue: 3, 580 - 584, 30.09.2020
https://doi.org/10.21541/apjes.637368

Abstract

Biyokoruma, çeşitli formlarda biyomoleküler terapötik
ajanların tıpta pratik kullanım bulmasını sağlayan kritik bir teknik ve
bilimsel araştırma alanı olmuştur. Temelini biyomimikriden alan biyomolekülleri
stabilize eden çözümlerin çalışma prensipleri bilimsel ilgi odağı olmuştur. Bu
çalışmada, lizozimin proteinlerin biyolojik olarak korunmasında sıkça
kullanılan iki çözücü olan gliserol ve trehaloz içerisindeki davranışlarını, bu
çözücülerin birbirinden farklı olan dinamik bastırma yeteneklerinin mikroskobik
kökenlerini belirlemek amacıyla inceledik. Gliserolün düşük sıcaklıklarda
trehaloza (trehalozun daha derin bir camsı halde olmasına rağmen) üstün
olduğunu, trehalozun ise yüksek sıcaklıklarda daha etkin olduğunu gözlemledik.
Bu sonucun kökeninin protein ve çözücü arasındaki moleküller arası hidrojen
bağlarının farklı sıcaklık bağımlılıklarına sahip oldukları sonucuna vardık.

References

  • [1] M. Tollinger, K. A. Crowhurst, L. E. Kay, and J. D. Forman-Kay, “Site-specific contributions to the pH dependence of protein stability,” Proc. Natl. Acad. Sci., vol. 100, no. 8, pp. 4545–4550, Apr. 2003.
  • [2] T. J. Magliery and L. Regan, “Combinatorial approaches to protein stability and structure,” Eur. J. Biochem., vol. 271, no. 9, pp. 1595–1608, May 2004.
  • [3] P. H. Yancey, “Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses,” J. Exp. Biol., vol. 208, no. 15, pp. 2819–2830, Aug. 2005.
  • [4] Mei Yang-woytowitz, Charles Yu, and Timothy Wiles, “Kits for the detection of beta-lactamases,” 8389234.
  • [5] V. R. Garigapati, D. Su, R. Khanzada, and S. J. Sawamura, “Protein stabilization formulations,” US8435943B2, 07-May-2013.
  • [6] Ali Eroglu, “Compositions and Methods for Biopreservation,” US20190098891A1, 2018.
  • [7] H. Faghihi, S. Merrikhihaghi, A. Ruholamini Najafabadi, V. Ramezani, S. Sardari, and A. Vatanara, “A Comparative Study to Evaluate the Effect of Different Carbohydrates on the Stability of Immunoglobulin G during Lyophilization and Following Storage,” Pharm. Sci., vol. 22, no. 4, pp. 251–259, Dec. 2016.
  • [8] K. Gekko and S. N. Timasheff, “Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures,” Biochemistry, vol. 20, no. 16, pp. 4667–4676, Aug. 1981.
  • [9] M. Uritani, M. Takai, and K. Yoshinaga, “Protective effect of disaccharides on restriction endonucleases during drying under vacuum1,” J. Biochem. (Tokyo), vol. 117, no. 4, pp. 774–779, Apr. 1995.
  • [10] R. B. Gregory, Ed., Protein-solvent interactions. New York, N.Y: M. Dekker, 1995.
  • [11] G. M. Sastry and N. Agmon, “Trehalose prevents myoglobin collapse and preserves its internal mobility,” Biochemistry, vol. 36, no. 23, pp. 7097–7108, Jun. 1997.
  • [12] A. Ansari et al., “Protein states and proteinquakes.,” Proc. Natl. Acad. Sci., vol. 82, no. 15, pp. 5000–5004, Aug. 1985.
  • [13] G. Caliskan et al., “Protein and solvent dynamics: How strongly are they coupled?,” J. Chem. Phys., vol. 121, no. 4, pp. 1978–1983, Jul. 2004.
  • [14] T. E. Dirama, G. A. Carri, and A. P. Sokolov, “Coupling between lysozyme and glycerol dynamics: Microscopic insights from molecular-dynamics simulations,” J. Chem. Phys., vol. 122, no. 24, p. 244910, Jun. 2005.
  • [15] T. E. Dirama, J. E. Curtis, G. A. Carri, and A. P. Sokolov, “Coupling between lysozyme and trehalose dynamics: Microscopic insights from molecular-dynamics simulations,” J. Chem. Phys., vol. 124, no. 3, p. 034901, Jan. 2006.
  • [16] David A Case, TA Darden, and J. W. Caldwell, “Amber 9,” Univ. Calif. San Franc., vol. 45, 2006.
  • [17] J. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman, and D. A. Case, “Development and testing of a general amber force field,” J. Comput. Chem., vol. 25, no. 9, pp. 1157–1174, Jul. 2004.
  • [18] “Frisch, M.J., Trucks, G.W., Schlegel, H.B., et al., (2004) Gaussian 03, revision E. 01, Gaussian Inc., Wallingford CT. - References - Scientific Research Publishing.” [Online]. Available: http://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=631962. [Accessed: 23-Jul-2019].
  • [19] M. T. Cicerone, A. Tellington, L. Trost, and A. Sokolov, “Substantially improved stability of biological agents in dried form the role of glassy dynamics in preservation of biopharmaceuticals,” Bioprocess Int., vol. 1, no. 36, pp. 36–47, 2003.
  • [20] D. A. Waller, “Protein folding,” Biochem. Educ., vol. 21, no. 1, p. 50, Jan. 1993.
  • [21] T. Ackermann, “C. L. Brooks III, M. Karplus, B. M. Pettitt. Proteins: A Theoretical Perspective of Dynamics, Structure and Thermodynamics, Volume LXXI, in: Advances in Chemical Physics, John Wiley & Sons, New York 1988. 259 Seiten, Preis: US $ 65.25,” Berichte Bunsenges. Für Phys. Chem., vol. 94, no. 1, pp. 96–96, Jan. 1990.
  • [22] R. V. Dunn, V. Réat, J. Finney, M. Ferrand, J. C. Smith, and R. M. Daniel, “Enzyme activity and dynamics: xylanase activity in the absence of fast anharmonic dynamics,” Biochem. J., vol. 346, no. 2, p. 355, Mar. 2000.
  • [23] P. W. Fenimore, H. Frauenfelder, B. H. McMahon, and R. D. Young, “Bulk-solvent and hydration-shell fluctuations, similar to - and -fluctuations in glasses, control protein motions and functions,” Proc. Natl. Acad. Sci., vol. 101, no. 40, pp. 14408–14413, Oct. 2004.
  • [24] M. T. Cicerone and C. L. Soles, “Fast dynamics and stabilization of proteins: binary glasses of trehalose and glycerol,” Biophys. J., vol. 86, no. 6, pp. 3836–3845, Jun. 2004.
  • [25] W. S. Doster and M. Settles, “The dynamical transition in proteins: the role of hydrogen bonds,” in Hydration Processes in Biology: Theoretical and Experimental Approaches, M.-C. Bellissent-Funel., vol. 305, Berlin: IOS Press, pp. 177–191.
  • [26] M. Tarek and D. J. Tobias, “Role of Protein-Water Hydrogen Bond Dynamics in the Protein Dynamical Transition,” Phys. Rev. Lett., vol. 88, no. 13, p. 138101, Mar. 2002.
  • [27] M. Mezei and D. L. Beveridge, “Theoretical studies of hydrogen bonding in liquid water and dilute aqueous solutions,” J. Chem. Phys., vol. 74, no. 1, pp. 622–632, Jan. 1981.
There are 27 citations in total.

Details

Primary Language English
Subjects Engineering
Journal Section Articles
Authors

Taner Dirama 0000-0003-1975-6505

Publication Date September 30, 2020
Submission Date October 23, 2019
Published in Issue Year 2020 Volume: 8 Issue: 3

Cite

IEEE T. Dirama, “Physical Insights into the Bio-preservation of Proteins by Glassy Solvents: Why is Glycerol better than Trehalose at low Temperatures?”, APJES, vol. 8, no. 3, pp. 580–584, 2020, doi: 10.21541/apjes.637368.