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Impact of hydrodynamic interactions on protein folding rates depends on temperature

Fabio C. Zegarra1,2, Dirar Homouz1,2,3, Yossi Eliaz1,2, Andrei G. Gasic1,2, and Margaret S. Cheung1,2,*

  • 1Department of Physics, University of Houston, Houston, Texas 77204, USA
  • 2Center for Theoretical Biological Physics, Rice University, Houston, Texas 77005, USA
  • 3Khalifa University of Science and Technology, Department of Physics, P.O. Box 127788, Abu Dhabi, United Arab Emirates

  • *Corresponding author: mscheung@uh.edu
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Phys. Rev. E 97, 032402 – Published 5 March, 2018

DOI: https://doi.org/10.1103/PhysRevE.97.032402

Abstract

We investigated the impact of hydrodynamic interactions (HI) on protein folding using a coarse-grained model. The extent of the impact of hydrodynamic interactions, whether it accelerates, retards, or has no effect on protein folding, has been controversial. Together with a theoretical framework of the energy landscape theory (ELT) for protein folding that describes the dynamics of the collective motion with a single reaction coordinate across a folding barrier, we compared the kinetic effects of HI on the folding rates of two protein models that use a chain of single beads with distinctive topologies: a 64-residue α/β chymotrypsin inhibitor 2 (CI2) protein, and a 57-residue β-barrel α-spectrin Src-homology 3 domain (SH3) protein. When comparing the protein folding kinetics simulated with Brownian dynamics in the presence of HI to that in the absence of HI, we find that the effect of HI on protein folding appears to have a “crossover” behavior about the folding temperature. This means that at a temperature greater than the folding temperature, the enhanced friction from the hydrodynamic solvents between the beads in an unfolded configuration results in lowered folding rate; conversely, at a temperature lower than the folding temperature, HI accelerates folding by the backflow of solvent toward the folded configuration of a protein. Additionally, the extent of acceleration depends on the topology of a protein: for a protein like CI2, where its folding nucleus is rather diffuse in a transition state, HI channels the formation of contacts by favoring a major folding pathway in a complex free energy landscape, thus accelerating folding. For a protein like SH3, where its folding nucleus is already specific and less diffuse, HI matters less at a temperature lower than the folding temperature. Our findings provide further theoretical insight to protein folding kinetic experiments and simulations.

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References (64)

  1. Y. Levy and J. N. Onuchic, Annu. Rev. Biophys. Biomol. Struct. 35, 389 (2006).
  2. Y. Goldtzvik, Z. Zhang, and D. Thirumalai, J. Phys. Chem. B 120, 2071 (2016).
  3. M. Chiricotto, S. Melchionna, P. Derreumaux, and F. Sterpone, J. Chem. Phys. 145, 035102 (2016).
  4. A. S. Mikhailov and R. Kapral, Proc. Natl. Acad. Sci. USA 112, E3639 (2015).
  5. E. Pitard, Eur. Phys. J. B 7, 665 (1999).
  6. Y. A. Kuznetsov, E. G. Timoshenko, and K. A. Dawson, J. Chem. Phys. 104, 3338 (1996).
  7. K. Kamata, T. Araki, and H. Tanaka, Phys. Rev. Lett. 102, 108303 (2009).
  8. R. W. Chang and A. Yethiraj, J. Chem. Phys. 114, 7688 (2001).
  9. S. Das and S. Chakraborty, J. Chem. Phys. 133, 174904 (2010).
  10. N. Kikuchi, A. Gent, and J. M. Yeomans, Eur. Phys. J. E 9, 63 (2002).
  11. T. T. Pham, M. Bajaj, and J. R. Prakash, Soft Matter 4, 1196 (2008).
  12. M. Cieplak and S. Niewieczerzal, J. Chem. Phys. 130, 124906 (2009).
  13. T. Frembgen-Kesner and A. H. Elcock, J. Chem. Theory Comput. 5, 242 (2009).
  14. A. G. Lipska, S. R. Seidman, A. K. Sieradzan, A. Gieldon, A. Liwo, and H. A. Scheraga, J. Chem. Phys. 144, 184110 (2016).
  15. N. Kikuchi, J. F. Ryder, C. M. Pooley, and J. M. Yeomans, Phys. Rev. E 71, 061804 (2005).
  16. J. N. Onuchic, H. Nymeyer, A. E. Garcia, J. Chahine, and N. D. Socci, Adv. Protein Chem. 53, 87 (2000).
  17. M. Oliveberg and P. G. Wolynes, Q. Rev. Biophys. 38, 245 (2005).
  18. J. D. Bryngelson and P. G. Wolynes, Proc. Natl. Acad. Sci. USA 84, 7524 (1987).
  19. P. E. Leopold, M. Montal, and J. N. Onuchic, Proc. Natl. Acad. Sci. USA 89, 8721 (1992).
  20. C. Clementi, H. Nymeyer, and J. N. Onuchic, J. Mol. Biol. 298, 937 (2000).
  21. Y. Harpaz, N. Elmasry, A. R. Fersht, and K. Henrick, Proc. Natl. Acad. Sci. USA 91, 311 (1994).
  22. A. Musacchio, M. Noble, R. Pauptit, R. Wierenga, and M. Saraste, Nature (London) 359, 851 (1992).
  23. N. V. Dokholyan, L. Li, F. Ding, and E. I. Shakhnovich, Proc. Natl. Acad. Sci. USA 99, 8637 (2002).
  24. T. Hoang and M. Cieplak, J. Chem. Phys. 113, 8319 (2000).
  25. T. R. Weikl and K. A. Dill, J. Mol. Biol. 332, 953 (2003).
  26. L. Wu, W. Li, F. Liu, J. Zhang, J. Wang, and W. Wang, J. Chem. Phys. 131, 065105 (2009).
  27. C. Camilloni, L. Sutto, D. Provasi, G. Tiana, and R. A. Broglia, Protein Sci. 17, 1424 (2008).
  28. D. L. Ermak and J. A. McCammon, J. Chem. Phys. 69, 1352 (1978).
  29. H. Nymeyer, N. D. Socci, and J. N. Onuchic, Proc. Natl. Acad. Sci. USA 97, 634 (2000).
  30. V. Sobolev, A. Sorokine, J. Prilusky, E. E. Abola, and M. Edelman, Bioinformatics 15, 327 (1999).
  31. W. X. Xu, Z. Z. Lai, R. J. Oliveira, V. B. P. Leite, and J. Wang, J. Phys. Chem. B 116, 5152 (2012).
  32. A. Stivala, M. Wybrow, A. Wirth, J. C. Whisstock, and P. J. Stuckey, Bioinformatics 27, 3315 (2011).
  33. W. Humphrey, A. Dalke, and K. Schulten, J. Mol. Graphics Modell. 14, 33 (1996).
  34. W. Kabsch and C. Sander, Biopolymers 22, 2577 (1983).
  35. L. S. Itzhaki, D. E. Otzen, and A. R. Fersht, J. Mol. Biol. 254, 260 (1995).
  36. S. L. Kazmirski, K. B. Wong, S. M. V. Freund, Y. J. Tan, A. R. Fersht, and V. Daggett, Proc. Natl. Acad. Sci. USA 98, 4349 (2001).
  37. J. C. Martinez, M. T. Pisabarro, and L. Serrano, Nat. Struct. Biol. 5, 721 (1998).
  38. V. P. Grantcharova, D. S. Riddle, J. V. Santiago, and D. Baker, Nat. Struct. Biol. 5, 714 (1998).
  39. T. Ando and J. Skolnick, Proc. Natl. Acad. Sci. USA 107, 18457 (2010).
  40. J. Rotne and S. Prager, J. Chem. Phys. 50, 4831 (1969).
  41. H. Yamakawa, J. Chem. Phys. 53, 436 (1970).
  42. Y. Sugita and Y. Okamoto, Chem. Phys. Lett. 314, 141 (1999).
  43. N. Metropolis, A. W. Rosenbluth, M. N. Rosenbluth, A. H. Teller, and E. Teller, J. Chem. Phys. 21, 1087 (1953).
  44. J. D. Chodera, W. C. Swope, J. W. Pitera, C. Seok, and K. A. Dill, J. Chem. Theory Comput. 3, 26 (2007).
  45. P. C. Whitford, S. C. Blanchard, J. H. D. Cate, and K. Y. Sanbonmatsu, PLoS Comput. Biol. 9, e1003003 (2013).
  46. N. D. Socci, J. N. Onuchic, and P. G. Wolynes, J. Chem. Phys. 104, 5860 (1996).
  47. J. D. Bryngelson and P. G. Wolynes, J. Phys. Chem. 93, 6902 (1989).
  48. P. Hanggi, P. Talkner, and M. Borkovec, Rev. Mod. Phys. 62, 251 (1990).
  49. S. V. Krivov, PLoS Comput. Biol. 6, e1000938 (2010).
  50. T. Neusius, I. Daidone, I. M. Sokolov, and J. C. Smith, Phys. Rev. Lett. 100, 188103 (2008).
  51. L. Li, L. A. Mirny, and E. I. Shakhnovich, Nat. Struct. Biol. 7, 336 (2000).
  52. K. Lindorff-Larsen, S. Piana, R. O. Dror, and D. E. Shaw, Science 334, 517 (2011).
  53. V. S. Pande, Phys. Rev. Lett. 105, 198101 (2010).
  54. S. F. Chekmarev, A. Y. Palyanov, and M. Karplus, Phys. Rev. Lett. 100, 018107 (2008).
  55. H. Tanaka, J. Phys.: Condens. Matter 17, S2795 (2005).
  56. R. B. Best and G. Hummer, Proc. Natl. Acad. Sci. USA 107, 1088 (2010).
  57. W. Y. Yang and M. Gruebele, Biochemistry 43, 13018 (2004).
  58. B. Berger and T. Leighton, J. Comput. Biol. 5, 27 (1998).
  59. J. T. Ngo, J. Marks, and M. Karplus, in The Protein Folding Problem and Tertiary Structure Prediction, edited by K. Merz and S. M. LeGrand (Birkhäuser, Boston, 1994), p. 433.
  60. N. A. Denesyuk and J. D. Weeks, Phys. Rev. Lett. 102, 108101 (2009).
  61. G. Morrison, C. Hyeon, M. Hinczewski, and D. Thirumalai, Phys. Rev. Lett. 106, 138102 (2011).
  62. P. I. Zhuravlev, M. Hinczewski, S. Chakrabarti, S. Marqusee, and D. Thirumalai, Proc. Natl. Acad. Sci. USA 113, E715 (2016).
  63. K. Neupane, A. P. Manuel, and M. T. Woodside, Nat. Phys. 12, 700 (2016).
  64. S. E. Jackson, N. elMasry, and A. R. Fersht, Biochemistry 32, 11270 (1993).

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Phys. Rev. E 97, 032402– Published 5 March, 2018
  • Received 12 December 2017
Article part of CHORUS
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