The European Physical Journal Special Topics

, Volume 226, Issue 4, pp 627–638 | Cite as

Protein folding/unfolding in the presence of interacting macromolecular crowders

Open Access
Review
Part of the following topical collections:
  1. Recent Advances in Phase Transitions and Critical Phenomena

Abstract

Recent years have seen an increasing number of biophysical studies of proteins being conducted in cells and concentrated protein solutions. In these experiments, compared to dilute-solution data, both stabilization and destabilization of globular proteins have been observed, which cannot be explained in terms of volume exclusion alone. For a fundamental understanding of the observed effects, there is a need for computational modeling beyond the level of hard-sphere crowders. This mini-review discusses recent efforts to simulate folding/unfolding properties of proteins in the presence of explicit macromolecular crowders. A Monte Carlo-based approach by us is described, which we recently applied to study the equilibrium folding thermodynamics of two peptides in the presence of explicit protein crowders.

References

  1. 1.
    S.B. Zimmerman, S.O. Trach, J. Mol. Biol. 222, 599 (1991)CrossRefGoogle Scholar
  2. 2.
    F.X. Theillet, A. Binolfi, T. Frembgen-Kesner, K. Hingorani, M. Sarkar, C. Kyne, C. Li, P.B. Crowley, L. Gierasch, G.J. Pielak, A.H. Elcock, A. Gershenson, P. Selenko, Chem. Rev. 114, 6661 (2014)CrossRefGoogle Scholar
  3. 3.
    A.E. Smith, Z. Zhang, G.J. Pielak, C. Li, Curr. Opin. Struct. Biol. 30, 7 (2015)CrossRefGoogle Scholar
  4. 4.
    H.X. Zhou, FEBS Lett. 587, 1053 (2013)CrossRefGoogle Scholar
  5. 5.
    M. Feig, Y. Sugita, J. Mol. Graph. Model. 45, 144 (2013)CrossRefGoogle Scholar
  6. 6.
    R.J. Ellis, Trends Biochem. Sci. 26, 597 (2001)CrossRefGoogle Scholar
  7. 7.
    H.X. Zhou, G. Rivas, A.P. Minton, Annu. Rev. Biophys. 37, 375 (2008)CrossRefGoogle Scholar
  8. 8.
    M.S. Cheung, D. Klimov, D. Thirumalai, Proc. Natl. Acad. Sci. USA 102, 4753 (2005)ADSCrossRefGoogle Scholar
  9. 9.
    D.D.L. Minh, C.E. Chang, J. Trylska, V. Tozzini, J.A. McCammon, J. Am. Chem. Soc. 128, 6006 (2006)CrossRefGoogle Scholar
  10. 10.
    S. Qin, H.X. Zhou, Biophys. J. 97, 12 (2009)ADSCrossRefGoogle Scholar
  11. 11.
    B.R. Jefferys, L.A. Kelley, M.J.E. Sternberg, J. Mol. Biol. 397, 1329 (2010)CrossRefGoogle Scholar
  12. 12.
    D. Tsao, N.V. Dokholyan, Phys. Chem. Chem. Phys. 12, 3491 (2010)CrossRefGoogle Scholar
  13. 13.
    J. Mittal, R.B. Best, Biophys. J. 98, 315 (2010)ADSCrossRefGoogle Scholar
  14. 14.
    A. Samiotakis, M.S. Cheung, J. Chem. Phys. 135, 175101 (2011)ADSCrossRefGoogle Scholar
  15. 15.
    Q. Wang, M.S. Cheung, Biophys. J. 102, 2353 (2012)ADSCrossRefGoogle Scholar
  16. 16.
    S. Qin, H.X. Zhou, J. Phys. Chem. Lett. 4, 3429 (2013)CrossRefGoogle Scholar
  17. 17.
    H. Kang, P.A. Pincus, C. Hyeon, D. Thirumalai, Phys. Rev. Lett. 114, 068303 (2015)ADSCrossRefGoogle Scholar
  18. 18.
    D.C. Latshaw II, C.K. Hall, Biophys. J. 109, 124 (2015)ADSCrossRefGoogle Scholar
  19. 19.
    C.M. Miller, Y.C. Kim, J. Mittal, Biophys. J. 111, 28 (2016)ADSCrossRefGoogle Scholar
  20. 20.
    L. Stagg, S.Q. Zhang, M.S. Cheung, P. Wittung-Stafshede, Proc. Natl. Acad. Sci. USA 104, 18976 (2007)ADSCrossRefGoogle Scholar
  21. 21.
    J.M. Mouillon, S.K. Eriksson, P. Harryson, Plant Physiol. 148, 1925 (2008)CrossRefGoogle Scholar
  22. 22.
    C. Szasz, A. Alexa, K. Toth, M. Rakacs, J. Langowski, P. Tompa, Biochemistry 50, 5834 (2011)CrossRefGoogle Scholar
  23. 23.
    E.A. Cino, M. Karttunen, W.Y. Choy, PLOS One 7, e49876 (2012)ADSCrossRefGoogle Scholar
  24. 24.
    A.E. Smith, L.Z. Zhou, G.J. Pielak, Protein Sci. 24, 706 (2015)CrossRefGoogle Scholar
  25. 25.
    A.C. Miklos, M. Sarkar, Y. Wang, G.J. Pielak, J. Am. Chem. Soc. 133, 7116 (2011)CrossRefGoogle Scholar
  26. 26.
    I. Guzman, H. Gelman, J. Tai, M. Gruebele, J. Mol. Biol. 426, 11 (2014)CrossRefGoogle Scholar
  27. 27.
    J. Danielsson, X. Mu, L. Lang, H. Wang, A. Binolfi, F.X. Theillet, B. Bekei, D.T. Logan, P. Selenko, H. Wennerström, M. Oliveberg, Proc. Natl. Acad. Sci. USA 112, 12402 (2015)ADSCrossRefGoogle Scholar
  28. 28.
    A.E. Smith, L.Z. Zhou, A.H. Gorensek, M. Senske, G.J. Pielak, Proc. Natl. Acad. Sci. USA 113, 1725 (2016)ADSCrossRefGoogle Scholar
  29. 29.
    S.N. Timasheff, Proc. Natl. Acad. Sci. USA 99, 9721 (2002)ADSCrossRefGoogle Scholar
  30. 30.
    L. Sapir, D. Harries, Curr. Opin. Colloid Interface Sci. 20, 3 (2015)CrossRefGoogle Scholar
  31. 31.
    L. Hua, R. Zhou, D. Thirumalai, B.J. Berne, Proc. Natl. Acad. Sci. USA 105, 16928 (2008)ADSCrossRefGoogle Scholar
  32. 32.
    D.R. Canchi, D. Paschek, A.E. García, J. Am. Chem. Soc. 132, 2338 (2010)CrossRefGoogle Scholar
  33. 33.
    D. Horinek, R.R. Netz, J. Phys. Chem. A 115, 6125 (2011)CrossRefGoogle Scholar
  34. 34.
    B.J. Bennion, V. Daggett, Proc. Natl. Acad. Sci. USA 101, 6433 (2004)ADSCrossRefGoogle Scholar
  35. 35.
    M.V. Athawale, J.S. Dordick, S. Garde, Biophys. J. 89, 858 (2005)CrossRefGoogle Scholar
  36. 36.
    C.Y. Hu, G.C. Lynch, H. Kokubo, B.M. Pettitt, Proteins 78, 695 (2010)Google Scholar
  37. 37.
    D.R. Canchi, P. Jayasimha, D.C. Rau, G.I. Makhatadze, A.E. García, J. Phys. Chem. B 116, 12095 (2012)CrossRefGoogle Scholar
  38. 38.
    Z.A. Levine, L. Larini, N.E. LaPointe, S.C. Feinstein, J.E. Shea, Proc. Natl. Acad. Sci. USA 112, 2758 (2015)ADSCrossRefGoogle Scholar
  39. 39.
    C.P. Brangwynne, C.R. Eckmann, D.S. Courson, A. Rybarska, C. Hoege, J. Gharakhani, F. Julicher, A.A. Hyman, Science 324, 1729 (2009)ADSCrossRefGoogle Scholar
  40. 40.
    A.J. Wirth, M. Gruebele, BioEssays 35, 984 (2013)CrossRefGoogle Scholar
  41. 41.
    S. Qin, H.X. Zhou, Curr. Opin. Struct. Biol. 43, 28 (2017)CrossRefGoogle Scholar
  42. 42.
    A. Bille, B. Linse, S. Mohanty, A. Irbäck, J. Chem. Phys. 143, 175102 (2015)ADSCrossRefGoogle Scholar
  43. 43.
    A. Bille, S. Mohanty, A. Irbäck, J. Chem. Phys. 144, 175105 (2016)ADSCrossRefGoogle Scholar
  44. 44.
    A. Irbäck, S. Mohanty, J. Comput. Chem. 27, 1548 (2006)CrossRefGoogle Scholar
  45. 45.
    T. Ando, J. Skolnick, Proc. Natl. Acad. Sci. USA 107, 18457 (2010)ADSCrossRefGoogle Scholar
  46. 46.
    P. Mereghetti, R.C. Wade, J. Phys. Chem. B 116, 8523 (2012)CrossRefGoogle Scholar
  47. 47.
    S. Hasnain, C.L. McClendon, M.T. Hsu, M.P. Jacobson, P. Bandyopadhyay, PLOS One 9, e106466 (2014)ADSCrossRefGoogle Scholar
  48. 48.
    S. Kondrat, O. Zimmermann, W. Wiechert, E.v. Lieres, Phys. Biol. 12, 046003 (2015)ADSCrossRefGoogle Scholar
  49. 49.
    M. Feig, Y. Sugita, J. Phys. Chem. B 116, 599 (2012)CrossRefGoogle Scholar
  50. 50.
    K. Meister, S. Ebbinghaus, Y. Xu, J.G. Duman, A. DeVries, M. Gruebele, D.M. Leitner, M. Havenith, Proc. Natl. Acad. Sci. USA 110, 1617 (2013)ADSCrossRefGoogle Scholar
  51. 51.
    D.R. Canchi, A.E. García, Annu. Rev. Phys. Chem. 64, 273 (2013)ADSCrossRefGoogle Scholar
  52. 52.
    A.V. Predeus, S. Gul, S.M. Gopal, M. Feig, J. Phys. Chem. B 116, 8610 (2012)CrossRefGoogle Scholar
  53. 53.
    S. Kmiecik, D. Gront, M. Kolinski, L. Wieteska, A.E. Dawid, A. Kolinski, Chem. Rev. 116, 7898 (2016)CrossRefGoogle Scholar
  54. 54.
    F. Sterpone, P. Derreumaux, S. Melchionna, J. Chem. Theory Comput. 11, 1843 (2015)CrossRefGoogle Scholar
  55. 55.
    U.H.E. Hansmann, Chem. Phys. Lett. 281, 140 (1997)ADSCrossRefGoogle Scholar
  56. 56.
    Y. Sugita, Y. Okamoto, Chem. Phys. Lett. 314, 141 (1999)ADSCrossRefGoogle Scholar
  57. 57.
    S. Qin, D.D.L. Minh, J.A. McCammon, H.X. Zhou, J. Phys. Chem. Lett. 1, 107 (2010)CrossRefGoogle Scholar
  58. 58.
    S.R. McGuffee, A.H. Elcock, PLOS Comput. Biol. 6, e1000694 (2010)ADSCrossRefGoogle Scholar
  59. 59.
    S. Qin, J. Mittal, H.X. Zhou, Phys. Biol. 10, 045001 (2013)ADSCrossRefGoogle Scholar
  60. 60.
    N. Madras, A.D. Sokal, J. Stat. Phys. 50, 109 (1988)ADSCrossRefGoogle Scholar
  61. 61.
    H. Frauenkron, U. Bastolla, E. Gerstner, P. Grassberger, W. Nadler, Phys. Rev. Lett. 80, 3149 (1998)ADSCrossRefGoogle Scholar
  62. 62.
    M. Bachmann, W. Janke, Phys. Rev. Lett. 91, 208105 (2003)ADSCrossRefGoogle Scholar
  63. 63.
    M. Feig, R. Harada, T. Mori, I. Yu, K. Takahashi, Y. Sugita, J. Mol. Graph. Model. 58, 1 (2015)CrossRefGoogle Scholar
  64. 64.
    I. Yu, T. Mori, T. Ando, R. Harada, J. Jung, Y. Sugita, M. Feig, eLife 5, 18457 (2016)Google Scholar
  65. 65.
    R. Harada, N. Tochio, T. Kigawa, Y. Sugita, M. Feig, J. Am. Chem. Soc. 135, 3696 (2013)CrossRefGoogle Scholar
  66. 66.
    B. Macdonald, S. McCarley, S. Noeen, A.E. van Giessen, J. Phys. Chem. B 119, 2956 (2015)CrossRefGoogle Scholar
  67. 67.
    B. Macdonald, S. McCarley, S. Noeen, A.E. van Giessen, J. Phys. Chem. B 120, 650 (2016)CrossRefGoogle Scholar
  68. 68.
    J. Kim, J.E. Straub, T. Keyes, J. Phys. Chem. B 116, 8646 (2012)CrossRefGoogle Scholar
  69. 69.
    M. Candotti, M. Orozco, PLOS Comput. Biol. 12, e1005040 (2016)ADSCrossRefGoogle Scholar
  70. 70.
    J.W. Neidigh, R.M. Fesinmeyer, N.H. Andersen, Nat. Struct. Biol. 9, 425 (2002)CrossRefGoogle Scholar
  71. 71.
    R.M. Fesinmeyer, F.M. Hudson, N.H. Andersen, J. Am. Chem. Soc. 126, 7238 (2004)CrossRefGoogle Scholar
  72. 72.
    E. Moses, H.J. Hinz, J. Mol. Biol. 170, 765 (1983)CrossRefGoogle Scholar
  73. 73.
    A.M. Gronenborn, D.R. Filpula, N.Z. Essig, A. Achari, M. Whitlow, P.T. Wingfield, G.M. Clore, Science 253, 657 (1991)ADSCrossRefGoogle Scholar
  74. 74.
    A. Irbäck, S. Mitternacht, S. Mohanty, BMC Biophys. 2, 2 (2009)CrossRefGoogle Scholar
  75. 75.
    S. Mitternacht, S. Luccioli, A. Torcini, A. Imparato, A. Irbäck, Biophys. J. 96, 429 (2009)ADSCrossRefGoogle Scholar
  76. 76.
    S.AE. Jónsson, S. Mohanty, A. Irbäck, Proteins 80, 2169 (2012)CrossRefGoogle Scholar
  77. 77.
    S. Mohanty, J.H. Meinke, O. Zimmermann, Proteins 81, 1446 (2013)CrossRefGoogle Scholar
  78. 78.
    X. Cong, N. Casiraghi, G. Rossetti, S. Mohanty, G. Giachin, G. Legname, P. Carloni, J. Chem. Theory Comput. 9, 5158 (2013)CrossRefGoogle Scholar
  79. 79.
    A. Bille, S.Æ . Jónsson, M. Akke, A. Irbäck, J. Phys. Chem. B 117, 9194 (2013)CrossRefGoogle Scholar
  80. 80.
    S.Æ . Jónsson, S. Mitternacht, A. Irbäck, Biophys. J. 104, 2725 (2013)CrossRefGoogle Scholar
  81. 81.
    J. Petrlova, A. Bhattacherjee, W. Boomsma, S. Wallin, J.O. Lagerstedt, A. Irbäck, Protein Sci. 23, 1559 (2014)CrossRefGoogle Scholar
  82. 82.
    D. Li, S. Mohanty, A. Irbäck, S. Huo, PLOS Comput. Biol. 4, e1000238 (2008)ADSCrossRefGoogle Scholar
  83. 83.
    S. Mitternacht, I. Staneva, T. Härd, A. Irbäck, J. Mol. Biol. 410, 357 (2011)CrossRefGoogle Scholar
  84. 84.
    P. Tian, K. Lindorff-Larsen, W. Boomsma, M.H. Jensen, D.E. Otzen, PLOS One 11, e0146096 (2016)CrossRefGoogle Scholar
  85. 85.
    M. Bachmann, K. Goede, A. Beck-Sickinger, M. Grundmann, A. Irbäck, W. Janke, Angew. Chem. Int. Edit. 49, 9530 (2010)CrossRefGoogle Scholar
  86. 86.
    G. Favrin, A. Irbäck, F. Sjunnesson, J. Chem. Phys. 114, 8154 (2001)ADSCrossRefGoogle Scholar
  87. 87.
    R.H. Swendsen, J.S. Wang, Phys. Rev. Lett. 57, 2607 (1986)ADSMathSciNetCrossRefGoogle Scholar
  88. 88.
    B.K. Kay, M.P. Williamson, M. Sudol, FASEB J. 14, 231 (2000)Google Scholar

Copyright information

© The Author(s) 2017

Open Access This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Authors and Affiliations

  1. 1.Computational Biology & Biological Physics, Department of Astronomy and Theoretical Physics, Lund UniversityLundSweden
  2. 2.Institute for Advanced Simulation, Jülich Supercomputing Centre, Forschungszentrum JülichJülichGermany

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