Abstract
In the course of various biological processes, specific DNA-binding proteins must efficiently find a particular target sequence/protein or a damaged site on the DNA. DNA-binding proteins perform this task based on diffusion. Nevertheless, investigations over recent decades have found that the diffusion dynamics of DNA-binding proteins are generally complicated and, further, protein specific. In this review, we collect experimental and theoretical studies that quantify the diffusion dynamics of DNA-binding proteins and review them from the viewpoint of diffusion processes.
Similar content being viewed by others
References
A.D. Riggs, S. Bourgeois, M. Cohn, J. Mol. Biol. 53, 401 (1970)
O.G. Berg, R.B. Winter, P.H. Von Hippel, Biochemistry 20, 6929 (1981)
S.E. Halford, J.F. Marko, Nucl. Acids Res. 32, 3040 (2004)
A.B. Kolomeisky, Phys. Chem. Chem. Phys. 13, 2088 (2011)
H. Kabata, O. Kurosawa, I. Arai, M. Washizu, S.A. Margarson, R.E. Glass, N. Shimamoto, Science 262, 1561 (1993)
M. Barbi, C. Place, V. Popkov, M. Salerno, Phys. Rev. E 70, 041901 (2004a)
M. Barbi, C. Place, V. Popkov, M. Salerno, J. Biol. Phys. 30, 203 (2004b)
M. Slutsky, L.A. Mirny, Biophys. J. 87, 4021 (2004)
L. Mirny, M. Slutsky, Z. Wunderlich, A. Tafvizi, J. Leith, A. Kosmrlj, J. Phys. A 42, 434013 (2009)
M. Bauer, R. Metzler, PLoS One 8, e53956 (2013)
O. Pulkkinen, R. Metzler, Phys. Rev. Lett. 110, 198101 (2013)
M. Bauer, E.S. Rasmussen, M.A. Lomholt, R. Metzler, Sci. Rep. 5, 10072 (2015)
J. Gorman, E.C. Greene, Nat. Struct. Mol. Biol. 15, 768 (2008)
A. Tafvizi, F. Huang, J.S. Leith, A.R. Fersht, L.A. Mirny, A.M. van Oijen, Biophys. J. 95, L01 (2008)
A. Tafvizi, F. Huang, A.R. Fersht, L.A. Mirny, A.M. van Oijen, Proc. Natl. Acad. Sci. U.S.A. 108, 563 (2011)
J.S. Leith, A. Tafvizi, F. Huang, W.E. Uspal, P.S. Doyle, A.R. Fersht, L.A. Mirny, A.M. van Oijen, Proc. Natl. Acad. Sci. U.S.A. 109, 16552 (2012)
A. Murata, Y. Ito, R. Kashima, S. Kanbayashi, K. Nanatani, C. Igarashi, M. Okumura, K. Inaba, T. Tokino, S. Takahashi, K. Kamagata, J. Mol. Biol. 427, 2663 (2015)
Y. Itoh, A. Murata, S. Sakamoto, K. Nanatani, T. Wada, S. Takahashi, K. Kamagata, J. Mol. Biol. 428, 2916 (2016)
A. Murata, Y. Itoh, E. Mano, S. Kanbayashi, C. Igarashi, H. Takahashi, S. Takahashi, K. Kamagata, Biophys. J. 112, 2301 (2017)
D.R.G. Subekti, A. Murata, Y. Itoh, S. Fukuchi, H. Takahashi, S. Kanbayashi, S. Takahashi, K. Kamagata, Biochemistry 56, 4134 (2017)
M. Kong, L. Liu, X. Chen, K. Driscoll, P. Mao, S. Böhm, N. Kad, S. Watkins, K. Bernstein, J. Wyrick, J.H. Min, B. Van Houten, Mol. Cell 64, 376 (2016)
N.Y. Cheon, H.S. Kim, J.E. Yeo, O.D. Schärer, J.Y. Lee, Nucl. Acids Res. 47, 8337 (2019)
A. Granéli, C.C. Yeykal, R.B. Robertson, E.C. Greene, Proc. Natl. Acad. Sci. U.S.A. 103, 1221 (2006)
J.H. Kim, R.G. Larson, Nucl. Acids Res. 35, 3848 (2007)
I. Bonnet, A. Biebricher, P.L. Porté, C. Loverdo, O. Bénichou, R. Voituriez, C. Escudé, W. Wende, A. Pingoud, P. Desbiolles, Nucl. Acids Res. 36, 4118 (2008)
A. Biebricher, W. Wende, C. Escudé, A. Pingoud, P. Desbiolles, Biophys. J. 96, L50 (2009)
J. Dikić, C. Menges, S. Clarke, M. Kokkinidis, A. Pingoud, W. Wende, P. Desbiolles, Nucl. Acids Res. 40, 4064 (2012)
A.R. Dunn, N.M. Kad, S.R. Nelson, D.M. Warshaw, S.S. Wallace, Nucl. Acids Res. 39, 7487 (2011)
S.R. Nelson, A.R. Dunn, S.D. Kathe, D.M. Warshaw, S.S. Wallace, Proc. Natl. Acad. Sci. U.S.A. 111, E2091 (2014)
P.C. Blainey, A.M. van Oijen, A. Banerjee, G.L. Verdine, X.S. Xie, Proc. Natl. Acad. Sci. U.S.A. 103, 5752 (2006)
C.L. Vestergaard, P.C. Blainey, H. Flyvbjerg, Nucl. Acids Res. 46, 2446 (2018)
Y.M. Wang, R.H. Austin, E.C. Cox, Phys. Rev. Lett. 97, 048302 (2006)
E. Marklund, B. van Oosten, G. Mao, E. Amselem, K. Kipper, A. Sabantsev, A. Emmerich, D. Globisch, X. Zheng, L.C. Lehmann, O.G. Berg, M. Johansson, J. Elf, S. Deindl, Nature 583, 858 (2020)
J. Gorman, A. Chowdhury, J.A. Surtees, J. Shimada, D.R. Reichman, E. Alani, E.C. Greene, Mol. Cell 28, 359 (2007)
J. Gorman, A.J. Plys, M.L. Visnapuu, E. Alani, E.C. Greene, Nat. Struct. Mol. Biol. 17, 932 (2010)
M.W. Brown, Y. Kim, G.M. Williams, J.D. Huck, J.A. Surtees, I.J. Finkelstein, Nat. Commun. 7, 10607 (2016)
K. Kamagata, E. Mano, K. Ouchi, S. Kanbayashi, R.C. Johnson, J. Mol. Biol. 430, 655 (2018)
F. Wang, S. Redding, I.J. Finkelstein, J. Gorman, D.R. Reichman, E.C. Greene, Nat. Struct. Mol. Biol. 20, 174 (2013)
J. Lin, P. Countryman, N. Buncher, P. Kaur, L.E.Y. Zhang, G. Gibson, C. You, S.C. Watkins, J. Piehler, P.L. Opresko, N.M. Kad, H. Wang, Nucl. Acids Res. 42, 2493 (2014)
J. Lin, P. Countryman, H. Chen, H. Pan, Y. Fan, Y. Jiang, P. Kaur, W. Miao, G. Gurgel, C. You, J. Piehler, N.M. Kad, R. Riehn, P.L. Opresko, S. Smith, Y.J. Tao, H. Wang, Nucl. Acids Res. 44, 6363 (2016)
W.K. Cho, C. Jeong, D. Kim, M. Chang, K.M. Song, J. Hanne, C. Ban, R. Fishel, J.B. Lee, Structure 20, 1264 (2012)
C. Jeong, W.K. Cho, K.M. Song, C. Cook, T.Y. Yoon, C. Ban, R. Fishel, J.B. Lee, Nat. Struct. Mol. Biol. 18, 379 (2011)
N.M. Kad, H. Wang, G.G. Kennedy, D.M. Warshaw, B. Van Houten, Mol. Cell 37, 702 (2010)
H. Ghodke, H. Wang, C.L. Hsieh, S. Woldemeskel, S.C. Watkins, V. RapićOtrin, B. Van Houten, Proc. Natl. Acad. Sci. U.S.A. 111, E1862 (2014)
C.D. Hughes, H. Wang, H. Ghodke, M. Simons, A. Towheed, Y. Peng, B. Van Houten, N.M. Kad, Nucl. Acids Res. 41, 4901 (2013)
L. Liu, M. Kong, N.R. Gassman, B.D. Freudenthal, R. Prasad, S. Zhen, S.C. Watkins, S.H. Wilson, B. Van Houten, Nucl. Acids Res. 45, 12834 (2017)
L. Cuculis, Z. Abil, H. Zhao, C.M. Schroeder, Nat. Chem. Biol. 12, 831 (2016)
L. Cuculis, Z. Abil, H. Zhao, C.M. Schroeder, Nat. Commun. 6, 7277 (2015)
P.H. Richter, M. Eigen, Biophys. Chem. 2, 255 (1974)
O.G. Berg, C. Blomberg, Biophys. Chem. 4, 367 (1976)
P.H. von Hippel, Science 305, 350 (2004)
V. Dahirel, F. Paillusson, M. Jardat, M. Barbi, J.M. Victor, Phys. Rev. Lett. 102, 228101 (2009)
B. Bagchi, P.C. Blainey, X.S. Xie, J. Phys. Chem. B 112, 6282 (2008)
P.C. Blainey, G. Luo, S.C. Kou, W.F. Mangel, G.L. Verdine, B. Bagchi, X.S. Xie, Nat. Struct. Mol. Biol. 16, 1224 (2009)
R. Zwanzig, Proc. Natl. Acad. Sci. U.S.A. 85, 2029 (1988)
I. Goychuk, V.O. Kharchenko, Phys. Rev. Lett. 113, 100601 (2014)
I. Goychuk, Phys. Chem. Chem. Phys. 20, 24140 (2018)
S. Banerjee, R. Biswas, K. Seki, B. Bagchi, J. Chem. Phys. 141, 124105 (2014)
T. Terakawa, H. Kenzaki, S. Takada, J. Am. Chem. Soc. 134, 14555 (2012)
Y.M. Wang, R.H. Austin, Single-molecule imaging of LacI diffusing along nonspecific DNA. In Biophysics of DNA-Protein Interactions From Single Molecules to Biological Systems (Springer, New York, 2011), ed. by M.C. Williams, J.L. Maher, pp. 9–38
Y.G. Sinai, Theory Probab. Appl. 27, 256 (1983)
R.J. Ober, A. Tahmasbi, S. Ram, Z. Lin, E.S. Ward, IEEE Signal Process. Mag. 32, 58 (2015)
M. Hedglin, P.J. O’Brien, ACS Chem. Biol. 5, 427 (2010)
A. Pluciennik, P. Modrich, Proc. Natl. Acad. Sci. U.S.A. 104, 12709 (2007)
S. Halford, Biochem. Soc. Trans. 37, 343 (2009)
R.H. Porecha, J.T. Stivers, Proc. Natl. Acad. Sci. U.S.A. 105, 10791 (2008)
M.A. Lomholt, B. van den Broek, S.M.J. Kalisch, G.J.L. Wuite, R. Metzler, Proc. Natl. Acad. Sci. U.S.A. 106, 8204 (2009)
M.V. Smoluchowski, Z Phys. Chem. 92U, 129 (1918)
J. Haus, K.W. Kehr, Phys. Rep. 150, 263 (1987)
J.P. Bouchaud, A. Georges, Phys. Rep. 195, 127 (1990)
R. Metzler, J. Klafter, Phys. Rep. 339, 1 (2000)
A.G. Cherstvy, A.V. Chechkin, R. Metzler, New J. Phys. 15, 083039 (2013)
W. Wang, A.G. Cherstvy, A.V. Chechkin, S. Thapa, F. Seno, X. Liu, R. Metzler, J. Phys. A 53, 474001 (2020)
A.G. Cherstvy, R. Metzler, J. Stat. Mech. Theory Exp. 2015, P05010 (2015)
A.G. Cherstvy, R. Metzler, Phys. Chem. Chem. Phys. 15, 20220 (2013)
A.V. Chechkin, F. Seno, R. Metzler, I.M. Sokolov, Phys. Rev. X 7, 021002 (2017)
V. Sposini, A.V. Chechkin, F. Seno, G. Pagnini, R. Metzler, New J. Phys. 20, 043044 (2018)
N. Leibovich, E. Barkai, Phys. Rev. E 99, 042138 (2019)
A.G. Cherstvy, R. Metzler, Phys. Rev. E 90, 012134 (2014)
R. Salgado-García, Phys. A 453, 55 (2016)
B. Wang, S.M. Anthony, S.C. Bae, S. Granick, Proc. Natl. Acad. Sci. U.S.A. 106, 15160 (2009)
T.J. Lampo, S. Stylianidou, M.P. Backlund, P.A. Wiggins, A.J. Spakowitz, Biophys. J. 112, 532 (2017)
A.G. Cherstvy, S. Thapa, C.E. Wagner, R. Metzler, Soft. Matter 15, 2526 (2019)
B. Wang, J. Kuo, S.C. Bae, S. Granick, Nat. Mater. 11, 481 (2012)
S. Hapca, J.W. Crawford, I.M. Young, J.R. Soc, Interface 6, 111 (2009)
P. Chaudhuri, L. Berthier, W. Kob, Phys. Rev. Lett. 99, 060604 (2007)
S. Roldián-Vargas, L. Rovigatti, F. Sciortino, Soft Matter 13, 514 (2017)
T. Toyota, D.A. Head, C.F. Schmidt, D. Mizuno, Soft. Matter 7, 3234 (2011)
N. Samanta, R. Chakrabarti, Soft. Matter 12, 8554 (2016)
B.B. Mandelbrot, J.W. Van Ness, Siam Rev. 10, 422 (1968)
R. Metzler, J.H. Jeon, A.G. Cherstvy, E. Barkai, Phys. Chem. Chem. Phys. 16, 24128 (2014)
J.H. Jeon, R. Metzler, Phys. Rev. E 85, 021147 (2012)
J.H. Jeon, R. Metzler, Phys. Rev. E 81, 021103 (2010)
C. Beck, Phys. Rev. Lett. 87, 180601 (2001)
C. Beck, E.G.D. Cohen, Phys. A 322, 267 (2003)
M.V. Chubynsky, G.W. Slater, Phys. Rev. Lett. 113, 098302 (2014)
R.L. Blumberg Selinger, S. Havlin, F. Leyvraz, M. Schwartz, H.E. Stanley, Phys. Rev. A 40, 6755 (1989)
H. Kesten, Phys. A 138, 299 (1986)
I. Goychuk, V.O. Kharchenko, R. Metzler, Phys. Rev. E 96, 052134 (2017)
J.P. Kruse, W. Gu, Cell 137, 609 (2009)
C.J. Brown, S. Lain, C.S. Verma, A.R. Fersht, D.P. Lane, Nat. Rev. Cancer 9, 862 (2009)
R. Beckerman, C. Prives, Cold Spring Harb. Perspect. Biol. 2, a000935 (2010)
K.T. Bieging, S.S. Mello, L.D. Attardi, Nat. Rev. Cancer 14, 359 (2014)
A.C. Joerger, A.R. Fersht, Annu. Rev. Biochem. 77, 557 (2008)
M. Kitayner, H. Rozenberg, R. Rohs, O. Suad, D. Rabinovich, B. Honig, Z. Shakked, Nat. Struct. Mol. Biol. 17, 423 (2010)
R.L. Weinberg, S.M.V. Freund, D.B. Veprintsev, M. Bycroft, A.R. Fersht, J. Mol. Biol. 342, 801 (2004)
K. Kamagata, A. Murata, Y. Itoh, S. Takahashi, J. Photochem. Photobiol. C 30, 36 (2017)
A. Tafvizi, L.A. Mirny, A.M. van Oijen, ChemPhysChem 12, 1481 (2011)
M. Bustin, R. Reeves, Prog. Nucleic Acid Res. Mol. Biol. 54, 35 (1996)
M. Bustin, Mol. Cell. Biol. 19, 5237 (1999)
C. Tan, T. Terakawa, S. Takada, J. Am. Chem. Soc. 138, 8512 (2016)
F. Hanaoka, K. Sugasawa, D.N.A. Replication, Recombination, and Repair: Molecular Mechanisms and Pathology (Springer, New York, 2016)
P. Hammar, P. Leroy, A. Mahmutovic, E.G. Marklund, O.G. Berg, J. Elf, Science 336, 1595 (2012)
J.H. Min, N.P. Pavletich, Nature 449, 570 (2007)
X. Chen, Y. Velmurugu, G. Zheng, B. Park, Y. Shim, Y. Kim, L. Liu, B. Van Houten, C. He, A. Ansari, J.H. Min, Nat. Commun. 6, 5849 (2015)
K. Sugasawa, Mechanism and regulation of DNA damage recognition in mammalian nucleotide excision repair. In Enzymes (Academic Press, Cambridge, MA, 2019), ed. by L. Zhao, L.S. Kaguni, pp. 99–138
A. Sfeir, T. de Lange, Science 336, 593 (2012)
K.K. Bisht, Z. Daniloski, S. Smith, J. Cell Sci. 126, 3493 (2013)
A. Banerjee, W.L. Santos, G.L. Verdine, Science 311, 1153 (2006)
Y. Qi, M.C. Spong, K. Nam, M. Karplus, G.L. Verdine, J. Biol. Chem. 285, 1468 (2010)
C. Schick, C.T. Martin, Biochemistry 34, 666 (1995)
T. Li, H.H. Ho, M. Maslak, C. Schick, C.T. Martin, Biochemistry 35, 3722 (1996)
G.M.T. Cheetham, D. Jeruzalmi, T.A. Steitz, Nature 399, 80 (1999)
D. Imburgio, M. Rong, K. Ma, W.T. McAllister, Biochemistry 39, 10419 (2000)
T. Miyaguchi, T. Akimoto, E. Yamamoto, Phys. Rev. E 94, 012109 (2016)
T. Miyaguchi, T. Uneyama, T. Akimoto, Phys. Rev. E 100, 012116 (2019)
B. Bouvier, K. Zakrzewska, R. Lavery, Angew. Chem. 50, 6516 (2011)
M.J. Saxton, Biophys. J. 92, 1178 (2007)
A. Godec, A.V. Chechkin, E. Barkai, H. Kantz, R. Metzler, J. Phys. A 47, 492002 (2014)
V.O. Kharchenko, I. Goychuk, Phys. Rev. E 87, 052119 (2013)
Acknowledgements
This work was supported by the National Research Foundation (NRF) of Korea through No. 2018R1A6A3A11043366 (O.L.), No. 2020R1I1A1A01071790 (X.D.), and No. 2017K1A1A2013241 (J-H.J.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Park, S., Lee, Oc., Durang, X. et al. A mini-review of the diffusion dynamics of DNA-binding proteins: experiments and models. J. Korean Phys. Soc. 78, 408–426 (2021). https://doi.org/10.1007/s40042-021-00060-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40042-021-00060-y