Virus assembly and maturation: Auto-regulation through allosteric molecular switches

Journal of Molecular Biology

Volumn 425, Issue 9, 2013, Pages 1488-1496

  Domitrovic, Tatiana ^a   Movahed, Navid ^b   Bothner, Brian ^b   Matsui, Tsutomu ^c   Wang, Qiu ^d   Doerschuk, Peter C ^d   Johnson, John E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^d Cornell University   (United States)

Author keywords

hydrogen deuterium exchange; time resolved cryo EM; virus dynamic; virus maturation; virus structure

Indexed keywords

ALLOSTERISM; AMINO ACID SUBSTITUTION; CATALYSIS; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; NONHUMAN; NUDAURELIA CAPENSIS OMEGA VIRUS; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN QUATERNARY STRUCTURE; REVIEW; VIRUS; VIRUS ASSEMBLY; VIRUS CAPSID; X RAY CRYSTALLOGRAPHY;

ANIMALIA; MIRIDAE; NUDAURELIA CAPENSIS OMEGA VIRUS;

EID: 84876411185     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.02.021     Document Type: Review

References (35)

1. J. Monod, J.P. Changeux, and F. Jacob Allosteric proteins and cellular control systems J. Mol. Biol. 6 1963 306
2. J. Monod, J. Wyman, and J.P. Changeux On nature of allosteric transitions - a plausible model J. Mol. Biol. 12 1965 88
3. C. Packianathan, S.P. Katen, C.E. Dann, and A. Zlotnick Conformational changes in the hepatitis B virus core protein are consistent with a role for allostery in virus assembly J. Virol. 84 2010 1607 1615
4. E.C. Dykeman, P.G. Stockley, and R. Twarock Dynamic allostery controls coat protein conformer switching during MS2 phage assembly J. Mol. Biol. 395 2010 916 923
5. A. Zlotnick, and S. Mukhopadhyay Virus assembly, allostery and antivirals Trends Microbiol. 19 2011 14 23
6. O. Rolfsson, K. Toropova, N.A. Ranson, and P.G. Stockley Mutually-induced conformational switching of RNA and coat protein underpins efficient assembly of a viral capsid J. Mol. Biol. 401 2010 309 322
7. V.L. Morton, W. Burkitt, G. O'Connor, N.J. Stonehouse, P.G. Stockley, and A.E. Ashcroft RNA-induced conformational changes in a viral coat protein studied by hydrogen/deuterium exchange mass spectrometry Phys. Chem. Chem. Phys. 12 2010 13468 13475
8. C. Sanchez-San Martin, C.Y. Liu, and M. Kielian Dealing with low pH: entry and exit of alphaviruses and flaviviruses Trends Microbiol. 17 2009 514 521
9. M. Luo Influenza virus entry M.G. Rossmann, V.B. Rao, Viral Molecular Machines 726 2012 Springer-Verlag Berlin Berlin, NY 201 221
10. C.S. Adamson, K. Salzwedel, and E.O. Freed Virus maturation as a new HIV-1 therapeutic target Expert Opin. Ther. Targets 13 2009 895 908
11. D. Veesler, and J.E. Johnson Virus maturation D.C. Rees, Annual Review of Biophysics 41 2012 Annual Reviews, Inc. Palo Alto, CA 473 496
12. A. Odegard, M. Banerjee, and J.E. Johnson Flock house virus: a model system for understanding non-enveloped virus entry and membrane penetration Curr. Top. Microbiol. Immunol. 343 2010 1 22
13. T.M. Gallagher, and R.R. Rueckert Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus J. Virol. 62 1988 3399 3406
14. A.J. Barrett, N.D. Rawlings, and J.F. Woessner Handbook of Proteolytic Enzymes 2 2004 Elsevier Academic Press Amsterdam; Boston
15. A. Zlotnick, V.S. Reddy, R. Dasgupta, A. Schneemann, W.J. Ray Jr, R.R. Rueckert, and J.E. Johnson Capsid assembly in a family of animal viruses primes an autoproteolytic maturation that depends on a single aspartic acid residue J. Biol. Chem. 269 1994 13680 13684
16. A. Schneemann, T.M. Gallagher, and R.R. Rueckert Reconstitution of Flock House provirions: a model system for studying structure and assembly J. Virol. 68 1994 4547 4556
17. T.N. Hanzlik, and K.H. Gordon The Tetraviridae Adv. Virus Res. 48 1997 101 168
18. C. Helgstrand, S. Munshi, J.E. Johnson, and L. Liljas The refined structure of Nudaurelia capensis ω virus reveals control elements for a T = 4 capsid maturation Virology 318 2004 192 203
19. S. Munshi, L. Liljas, J. Cavarelli, W. Bomu, B. McKinney, V. Reddy, and J.E. Johnson The 2.8 angstrom structure of a T = 4 animal virus and its implications for membrane translocation of RNA J. Mol. Biol. 261 1996 1 10
20. D.J. Taylor, and J.E. Johnson Folding and particle assembly are disrupted by single-point mutations near the autocatalytic cleavage site of Nudaurelia capensis ω virus capsid protein Protein Sci. 14 2005 401 408
21. A. Routh, T. Domitrovic, and J.E. Johnson Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus Proc. Natl Acad. Sci. USA 109 2012 1907 1912
22. M.A. Canady, M. Tihova, T.N. Hanzlik, J.E. Johnson, and M. Yeager Large conformational changes in the maturation of a simple RNA virus, Nudaurelia capensis ω virus (NωV) J. Mol. Biol. 299 2000 573 584
23. T. Domitrovic, T. Matsui, and J.E. Johnson Dissecting quasi-equivalence in nonenveloped viruses: membrane disruption is promoted by lytic peptides released from subunit pentamers, not hexamers J. Virol. 86 2012 9976 9982
24. M.A. Canady, H. Tsuruta, and J.E. Johnson Analysis of rapid, large-scale protein quaternary structural changes: time-resolved X-ray solution scattering of Nudaurelia capensis ω virus (NωV) maturation J. Mol. Biol. 311 2001 803 814
25. T. Matsui, H. Tsuruta, and J.E. Johnson Balanced electrostatic and structural forces guide the large conformational change associated with maturation of T = 4 virus Biophys. J. 98 2010 1337 1343
26. T. Matsui, G. Lander, and J.E. Johnson Characterization of large conformational changes and autoproteolysis in the maturation of a T = 4 virus capsid J. Virol. 83 2009 1126 1134
27. D.J. Taylor, N.K. Krishna, M.A. Canady, A. Schneemann, and J.E. Johnson Large-scale, pH-dependent, quaternary structure changes in an RNA virus capsid are reversible in the absence of subunit autoproteolysis J. Virol. 76 2002 9972 9980
28. D. Kern, and E.R.P. Zuiderweg The role of dynamics in allosteric regulation Curr. Opin. Struct. Biol. 13 2003 748 757
29. Q. Wang, T. Matsui, T. Domitrovic, Y. Zheng, P.C. Doerschuk, and J.E. Johnson Dynamics in cryo EM reconstructions visualized with maximum-likelihood derived variance maps J. Struct. Biol. 181 2012 195 206
30. P.A. Penczek, M. Kimmel, and C.M. Spahn Identifying conformational states of macromolecules by eigen-analysis of resampled cryo-EM images Structure 19 2011 1582 1590
31. T. Matsui, G.C. Lander, R. Khayat, and J.E. Johnson Subunits fold at position-dependent rates during maturation of a eukaryotic RNA virus Proc. Natl Acad. Sci. USA 107 2010 14111 14115
32. J. Tang, K.K. Lee, B. Bothner, T.S. Baker, M. Yeager, and J.E. Johnson Dynamics and stability in maturation of a T = 4 virus J. Mol. Biol. 392 2009 803 812
33. T.S. Li, J.E. Johnson, and G.J. Thomas Raman dynamic probe of hydrogen exchange in bean pod mottle virus: base-specific retardation of exchange in packaged ssRNA Biophys. J. 65 1993 1963 1972
34. W.H. Roos, R. Bruinsma, and G.J.L. Wuite Physical virology Nat. Phys. 6 2010 733 743
35. D.L. Caspar Movement and self-control in protein assemblies. Quasi-equivalence revisited Biophys. J. 32 1980 103 138