Abstract
In the last decades, various biophysical techniques have been developed to provide more detailed pictures of biological systems of interest. Virus is one of the systems where these new approaches have been most successful. Different stages of the viral replication cycle have been probed with a multitude of biophysical approaches, producing numerous novel findings. To do so, researchers adopted various biophysical techniques best suited to understand the multifarious mechanisms of viral replication. Here, we review biophysical studies on virus during the last decades. This paper aims to be a guide for physicists who are interested in applying their techniques to viruses, so we emphasize preferable experimental methods and their capabilities in the context of virus research. We also provide a brief introduction to the viral replication cycle to help readers understand relevant questions in the field.
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References
E.M. Campbell, T.J. Hope, Trends. Microbiol. 16, 580 (2008)
T. Samji, Yale J. Biol. Med. 82, 153 (2009)
C.W. Kim, K.M. Chang, Clin. Mol. Hepatol. 19, 17 (2013)
U.F. Greber, M. Way, Cell 124, 741 (2006)
B. Brandenburg, X. Zhuang, Nat. Rev. Microbiol. 5, 197 (2007)
R. Fuchs, D. Blaas, Adv. Virol. 2012, 13 (2012)
W.I. Sundquist, H.G. Krausslich, Cold Spring Harb. Perspect. Med. 2, a006924 (2012)
P. Kukura, H. Ewers, C. Muller, A. Renn, A. Helenius et al., Nat. Methods 6, 923 (2009)
G. Seisenberger, M.U. Ried, T. Endreß, H. Büning, M. Hallek et al., Science 294, 1929 (2001)
S.L. Liu, Z.L. Zhang, Z.Q. Tian, H.S. Zhao, H. Liu et al., ACS Nano 6, 141 (2012)
K.I. Joo, Y. Lei, C.L. Lee, J. Lo, J. Xie et al., ACS Nano 2, 1553 (2008)
L. Gao, L. Shao, C.D. Higgins, J.S. Poulton, M. Peifer et al., Cell 151, 1370 (2012)
E.A. Abbondanzieri, G. Bokinsky, J.W. Rausch, J.X. Zhang, S.F. Le Grice et al., Nature 453, 184 (2008)
D.K. Das, R. Govindan, I. Nikić-Spiegel, F. Krammer, E.A. Lemke et al., Cell 174, 926 (2018)
M. Lu, X. Ma, L.R. Castillo-Menendez, J. Gorman, N. Alsahafi et al., Nature 568, 415 (2019)
S.J. Pond, W.K. Ridgeway, R. Robertson, J. Wang, D.P. Millar, Proc. Natl. Acad. Sci. USA 106, 1404 (2009)
N. Liu, B. Peng, Y. Lin, Z. Su, Z. Niu et al., J. Am. Chem. Soc. 132, 11036 (2010)
S. Myong, M.M. Bruno, A.M. Pyle, T. Ha, Science 317, 513 (2007)
S. Liu, E.A. Abbondanzieri, J.W. Rausch, S.F. Le Grice, X. Zhuang, Science 322, 1092 (2008)
G. Chen, K.Y. Chang, M.Y. Chou, C. Bustamante, I. Tinoco Jr., Proc. Natl. Acad. Sci. USA 106, 12706 (2009)
W. Cheng, S. Dumont, I. Tinoco Jr., C. Bustamante, Proc. Natl. Acad. Sci. USA 104, 13954 (2007)
C. Bustamante, W. Cheng, Y.X. Mejia, Cell 144, 480 (2011)
T.M. Dobrowsky, Y. Zhou, S.X. Sun, R.F. Siliciano, D. Wirtz, J. Virol. 82, 7022 (2008)
C. Rankl, F. Kienberger, L. Wildling, J. Wruss, H.J. Gruber et al., Proc. Natl. Acad. Sci. USA 105, 17778 (2008)
M. Gladnikoff, I. Rousso, Biophys. J. 94, 320 (2008)
F. Kienberger, R. Zhu, C. Rankl, H.J. Gruber, D. Blaas et al., Methods Enzymol. 475, 515 (2010)
S.D. Conner, S.L. Schmid, Nature 422, 37 (2003)
R.P. Subramanian, R.J. Geraghty, Proc. Natl. Acad. Sci. USA 104, 2903 (2007)
M.G. Sebestyen, V.G. Budker, T. Budker, V.M. Subbotin, G. Zhang et al., J. Gene Med. 8, 852 (2006)
E. Rothenberg, L.A. Sepúlveda, S.O. Skinner, L. Zeng, P.R. Selvin et al., Biophys. J. 100, 2875 (2011)
H. Ewers, A.E. Smith, I.F. Sbalzarini, H. Lilie, P. Koumoutsakos et al., Proc. Natl. Acad. Sci. USA 102, 15110 (2005)
J. Potel, P. Rassam, C. Montpellier, L. Kaestner, E. Werkmeister et al., Cell Microbiol. 15, 1234 (2013)
S. Bour, R. Geleziunas, M.A. Wainberg, Microbiol. Rev. 59, 63 (1995)
C. Sieben, C. Kappel, R. Zhu, A. Wozniak, C. Rankl et al., Proc. Natl. Acad. Sci. USA 109, 13626 (2012)
N.K. Sauter, J.E. Hanson, G.D. Glick, J.H. Brown, R.L. Crowther et al., Biochemistry 31, 9609 (1992)
M.J. Rust, M. Lakadamyali, F. Zhang, X. Zhuang, Nat. Struct. Mol. Biol. 11, 567 (2004)
D.L. Floyd, J.R. Ragains, J.J. Skehel, S.C. Harrison, A.M. van Oijen, Proc. Natl. Acad. Sci. USA 105, 15382 (2008)
K. Miyauchi, Y. Kim, O. Latinovic, V. Morozov, G.B. Melikyan, Cell 137, 433 (2009)
T. Ivanovic, J.L. Choi, S.P. Whelan, A.M. van Oijen, S.C. Harrison, eLife 2, e00333 (2013)
X. Ma, M. Lu, J. Gorman, D.S. Terry, X. Hong et al., eLife 7, e34271 (2018)
P. Grayson, L. Han, T. Winther, R. Phillips, Proc. Natl. Acad. Sci. USA 104, 14652 (2007)
P.K. Purohit, J. Kondev, R. Phillips, Proc. Natl. Acad. Sci. USA 100, 3173 (2003)
M.E. Fairman-Williams, E. Jankowsky, J. Mol. Biol. 415, 819 (2012)
C.-T. Lin, F. Tritschler, K.S. Lee, M. Gu, C.M. Rice et al., Protein Sci. 26, 1391 (2017)
A.J.W. te Velthuis, N.C. Robb, A.N. Kapanidis, E. Fodor, Nat. Microbiol. 1, 16029 (2016)
N.C. Robb, A.J. Te Velthuis, R. Wieneke, R. Tampé, T. Cordes et al., Nucleic Acids Res. 44, 10304 (2016)
G. Cosa, E.J. Harbron, Y. Zeng, H.W. Liu, D.B. O’Connor et al., Biophys. J. 87, 2759 (2004)
H.W. Liu, Y. Zeng, C.F. Landes, Y.J. Kim, Y. Zhu et al., Proc. Natl. Acad. Sci. USA 104, 5261 (2007)
N. Beerens, M.D. Jepsen, V. Nechyporuk-Zloy, A.C. Kruger, J.L. Darlix et al., RNA 19, 517 (2013)
H. Wang, K. Musier-Forsyth, C. Falk, P.F. Barbara, J. Phys. Chem. B 117, 4183 (2013)
K.M. Stewart-Maynard, M. Cruceanu, F. Wang, M.N. Vo, R.J. Gorelick et al., J. Virol. 82, 10129 (2008)
M. Cruceanu, R.J. Gorelick, K. Musier-Forsyth, I. Rouzina, M.C. Williams, J. Mol. Biol. 363, 867 (2006)
D.F. Qualley, K.M. Stewart-Maynard, F. Wang, M. Mitra, R.J. Gorelick et al., J. Biol. Chem. 285, 295 (2010)
S. Malkusch, W. Muranyi, B. Muller, H.G. Krausslich, M. Heilemann, Histochem. Cell Biol. 139, 173 (2013)
S. Kim, C.M. Schroeder, X.S. Xie, J. Mol. Biol. 395, 995 (2010)
R.M. Robertson-Anderson, J. Wang, S.P. Edgcomb, A.B. Carmel, J.R. Williamson et al., J. Mol. Biol. 410, 959 (2011)
Y.R. Chemla, D.E. Smith, Adv. Exp. Med. Biol. 726, 549 (2012)
D.E. Smith, S.J. Tans, S.B. Smith, S. Grimes, D.L. Anderson et al., Nature 413, 748 (2001)
D.N. Fuller, D.M. Raymer, V.I. Kottadiel, V.B. Rao, D.E. Smith, Proc. Natl. Acad. Sci. USA 104, 16868 (2007)
Y.R. Chemla, K. Aathavan, J. Michaelis, S. Grimes, P.J. Jardine et al., Cell 122, 683 (2005)
J.M. Tsay, J. Sippy, M. Feiss, D.E. Smith, Proc. Natl. Acad. Sci. USA 106, 14355 (2009)
J.M. Tsay, J. Sippy, D. DelToro, B.T. Andrews, B. Draper et al., J. Biol. Chem. 285, 24282 (2010)
V.I. Kottadiel, V.B. Rao, Y.R. Chemla, Proc. Natl. Acad. Sci. USA 109, 20000 (2012)
R. Vafabakhsh, K. Kondabagil, T. Earnest, K.S. Lee, Z. Zhang et al., Proc. Natl. Acad. Sci. USA 111, 15096 (2014)
V.B. Rao, M. Feiss, Annu. Rev. Genet. 42, 647 (2008)
K. Ray, J. Ma, M. Oram, J.R. Lakowicz, L.W. Black, J. Mol. Biol. 395, 1102 (2010)
C. Chen, S. Sheng, Z. Shao, P. Guo, J. Biol. Chem. 275, 17510 (2000)
D. Shu, H. Zhang, R. Petrenko, J. Meller, P. Guo, ACS Nano 4, 6843 (2010)
A. Borodavka, R. Tuma, P.G. Stockley, Proc. Natl. Acad. Sci. USA 109, 15769 (2012)
A. Borodavka, R. Tuma, P.G. Stockley, RNA Biol 10, 481 (2013)
I.A. Andreev, S. Hyon Kim, N.O. Kalinina, D.V. Rakitina, A.G. Fitzgerald et al., J. Mol. Biol. 339, 1041 (2004)
B.N. Fields, D.M. Knipe, P.M. Howley, Fields’ Virology, 5th edn. (Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, 2007).
N. Takizawa, K. Watanabe, K. Nouno, N. Kobayashi, K. Nagata, Microbes Infect. 8, 823 (2006)
Y.Y. Chou, R. Vafabakhsh, S. Doganay, Q. Gao, T. Ha et al., Proc. Natl. Acad. Sci. USA 109, 9101 (2012)
Y.Y. Chou, N.S. Heaton, Q. Gao, P. Palese, R. Singer et al., PLoS Pathog. 9, e1003358 (2013)
Y. Yang, N. Qu, J. Tan, M.N. Rushdi, C.J. Krueger et al., Proc. Natl. Acad. Sci. USA 115, 6721 (2018)
N. Pezeshkian, N.S. Groves, S.B. van Engelenburg, Proc. Natl. Acad. Sci. USA 116, 25269 (2019)
N. Jouvenet, P.D. Bieniasz, S.M. Simon, Nature 454, 236 (2008)
N. Jouvenet, S.M. Simon, P.D. Bieniasz, Proc. Natl. Acad. Sci. USA 106, 19114 (2009)
E. Adu-Gyamfi, M.A. Digman, E. Gratton, R.V. Stahelin, Biophys. J. 102, 2517 (2012)
M. Gladnikoff, E. Shimoni, N.S. Gov, I. Rousso, Biophys. J. 97, 2419 (2009)
G.Q. Tang, R. Roy, R.P. Bandwar, T. Ha, S.S. Patel, Proc. Natl. Acad. Sci. USA 106, 22175 (2009)
L.J. Friedman, J.P. Mumm, J. Gelles, Proc. Natl. Acad. Sci. USA 110, 9740 (2013)
Y. Cheng, R.M. Glaeser, E. Nogales, Cell 171, 1229 (2017)
S.A. Jones, S.H. Shim, J. He, X. Zhuang, Nat. Methods 8, 499 (2011)
S. Hohng, R. Zhou, M.K. Nahas, J. Yu, K. Schulten et al., Science 318, 279 (2007)
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The author gratefully acknowledges support by National Research Foundation of Korea grants 2017R1D1A1B03035671 and 2019R1C1C1007124.
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Lee, K.S. Biophysical approaches promote understanding of the viral replication cycle. J. Korean Phys. Soc. 78, 329–342 (2021). https://doi.org/10.1007/s40042-020-00030-w
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DOI: https://doi.org/10.1007/s40042-020-00030-w