Mechanics of bacteriophage maturation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 7, 2012, Pages 2342-2347

  Roos, Wouter H ^a   Gertsman, Ilya ^b,c   May, Eric R ^d   Brooks III, Charles L ^d   Johnson, John E ^b   Wuite, Gijs J L ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

AFM; Elastic network model; Nanoindentation; Normal mode analysis; Virus structural mechanics

Indexed keywords

ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE LAMBDA; BIOMECHANICS; CONTROLLED STUDY; CROSS LINKING; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; STRENGTH; VIROGENESIS; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS RESISTANCE; YOUNG MODULUS;

BACTERIOPHAGES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MICROSCOPY, ATOMIC FORCE;

ENTEROBACTERIA PHAGE LAMBDA; MIRIDAE;

EID: 84863115865     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109590109     Document Type: Article

References (51)

1. Baker ML, Jiang W, Rixon FJ, Chiu W (2005) Common ancestry of herpes viruses and tailed DNA bacteriophages. J Virol 79:14967-14970. (Pubitemid 41636294)
2. Johnson JE (2010) Virus particle maturation: insights into elegantly programmed nanomachines. Curr Opin Struct Biol 20:210-216.
3. Duda RL, et al. (1995) Structural transitions during bacteriophage HK97 head assembly. J Mol Biol 247:618-635.
4. Duda RL (1998) Protein chainmail: catenated protein in viral capsids. Cell 94:55-60.
5. Duda RL, Martincic K, Hendrix RW (1995) Genetic basis of bacteriophage HK97 prohead assembly. J Mol Biol 247:636-647.
6. Huang RK, et al. (2011) The prohead-I structure of bacteriophage HK97: implications for scaffold-mediated control of particle assembly and maturation. J Mol Biol 408:541-554.
7. Wikoff WR, et al. (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129-2133.
8. Conway JF, et al. (2001) Virus maturation involving large subunit rotations and local refolding. Science 292:744-748. (Pubitemid 32385549)
9. Lee KK, et al. (2008) Virus capsid expansion driven by the capture of mobile surface loops. Structure 16:1491-1502.
10. Gertsman I, et al. (2009) An unexpected twist in viral capsid maturation. Nature 458:646-650.
11. Steven AC, Heymann JB, Cheng NQ, Trus BL, Conway JF (2005) Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr Opin Struct Biol 15:227-236.
12. Ivanovska IL, et al. (2004) Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc Natl Acad Sci USA 101:7600-7605. (Pubitemid 38658075)
13. Michel JP, et al. (2006) Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc Natl Acad Sci USA 103:6184-6189.
14. Kol N, et al. (2006) Mechanical properties of murine leukemia virus particles: effect of maturation. Biophys J 91:767-774.
15. Carrasco C, et al. (2006) DNA-mediated anisotropic mechanical reinforcement of a virus. Proc Natl Acad Sci USA 103:13706-13711. (Pubitemid 44413971)
16. Roos WH, Bruinsma R, Wuite GJL (2010) Physical virology. Nat Phys 6:733-743.
17. Arkhipov A, Roos WH, Wuite GJ, Schulten K (2009) Elucidating the mechanism behind irreversible deformation of viral capsids. Biophys J 97:2061-2069.
18. Roos WH, et al. (2010) Squeezing protein shells: how continuum elastic models, molecular dynamics simulations, and experiments coalesce at the nanoscale. Biophys J 99:1175-1181.
19. May ER, Aggarwal A, Klug WS, Brooks CL, III (2011) Viral capsid equilibrium dynamics reveals nonuniform elastic properties. Biophys J 100:L59-L61.
20. May ER, Brooks CL, III (2011) Determination of viral capsid elastic properties from equilibrium thermal fluctuations. Phys Rev Lett 106:188101.
21. Ivanovska I, Wuite G, Jonsson B, Evilevitch A (2007) Internal DNA pressure modifies stability of WT phage. Proc Natl Acad Sci USA 104:9603-9608. (Pubitemid 47175313)
22. Evilevitch A, et al. (2011) Effects of salts on internal DNA pressure and mechanical properties of phage capsids. J Mol Biol 405:18-23.
23. Kuznetsov YG, Malkin AJ, Lucas RW, Plomp M, McPherson A (2001) Imaging of viruses by atomic force microscopy. J Gen Virol 82:2025-2034. (Pubitemid 32827582)
24. Baclayon M, Wuite GJL, RoosWH(2010) Imaging and manipulation of single viruses by atomic force microscopy. Soft Matter 6:5273-5285.
25. Gan L, et al. (2004) Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation. Mol Cell 14:559-569. (Pubitemid 38739080)
26. Landau LD, Lifshitz EM (1986) Theory of Elasticity (Elsevier, Oxford).
27. Gibbons MM, Klug WS (2007) Nonlinear finite-element analysis of nanoindentation of viral capsids. Phys Rev E 75:031901.
28. Wikoff WR, et al. (2006) Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography. J Struct Biol 153:300-306. (Pubitemid 43238322)
29. Tama F, Brooks CL, III (2006) Symmetry, form, and shape: guiding principles for robustness in macromolecular machines. Annu Rev Biophys Biomol Struct 35:115-133. (Pubitemid 43877372)
30. Bahar I, Rader AJ (2005) Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 15:586-592. (Pubitemid 41393491)
31. Rader AJ, Vlad DH, Bahar I (2005) Maturation dynamics of bacteriophage HK97 capsid. Structure 13:413-421. (Pubitemid 40342881)
32. Yang Z, Bahar I, Widom M (2009) Vibrational dynamics of icosahedrally symmetric biomolecular assemblies compared with predictions based on continuum elasticity. Biophys J 96:4438-4448.
33. Tama F, Brooks CL, III (2005) Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. J Mol Biol 345:299-314. (Pubitemid 39574852)
34. Gan L, et al. (2006) Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM. Structure 14:1655-1665. (Pubitemid 46107272)
35. Conway JF, Duda RL, Cheng N, Hendrix RW, Steven AC (1995) Proteolytic and conformational control of virus capsid maturation-the bacteriophage-HK97 system. J Mol Biol 253:86-99.
36. Dhillon EKS, Dhillon TS, Lai ANC, Linn S (1980) Host range, immunity and antigenic properties of lambdoid coliphage-HK97. J Gen Virol 50:217-220.
37. Casjens SR (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8:451-458.
38. Lander GC, et al. (2008) Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM. Structure 16:1399-1406.
39. Ross PD, et al. (2005) Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO J 24:1352-1363. (Pubitemid 40593056)
40. Morozov A, Rudnick J, Bruinsma R, KlugW(2010) Emerging Topics in Physical Virology, eds P Stockley and R Twarock (Imperial College Press, London).
41. Roos WH, et al. (2009) Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids. Proc Natl Acad Sci USA 106:9673-9678.
42. Roos WH, Ivanovska IL, Evilevitch A, Wuite GJL (2007) Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell Mol Life Sci 64:1484-1497. (Pubitemid 46954149)
43. Smith DE, et al. (2001) The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 413:748-752. (Pubitemid 33009954)
44. Carrasco C, et al. (2011) Built-in mechanical stress in viral shells. Biophys J 100:1100-1108.
45. Klug WS, et al. (2006) Failure of viral shells. Phys Rev Lett 97:228101.
46. Sader JE, Chon JWM, Mulvaney P (1999) Calibration of rectangular atomic force microscope cantilevers. Rev Sci Instrum 70:3967-3969. (Pubitemid 129589035)
47. Reddy VS, et al. (2001) Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses. J Virol 75:11943-11947. (Pubitemid 33115866)
48. Im WP, Lee MS, Brooks CL, III (2003) Generalized born model with a simple smoothing function. J Comput Chem 24:1691-1702.
49. Cagin T, Holder M, Pettitt BM (1991) A method for modeling icosahedral virions: rotational symmetry boundary-conditions. J Comput Chem 12:627-634.
50. Brooks BR, et al. (1983) Charmm-a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4:187-217.
51. Tama F, Gadea FX, Marques O, Sanejouand YH (2000) Building-block approach for determining low-frequency normal modes of macromolecules. Proteins 41:1-7. (Pubitemid 30666907)