Evidence for an electrostatic mechanism of force generation by the bacteriophage T4 DNA packaging motor

Nature Communications

Volumn 5, Issue , 2014, Pages

  Migliori, Amy D ^a   Keller, Nicholas ^a   Alam, Tanfis I ^b   Mahalingam, Marthandan ^b   Rao, Venigalla B ^b   Arya, Gaurav ^c   Smith, Douglas E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CATHOLIC UNIVERSITY OF AMERICA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GP17 PROTEIN; HELICASE; MICROSPHERE; MOLECULAR MOTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; STREPTAVIDIN; TUMOR ANTIGEN HELICASE; UNCLASSIFIED DRUG; GP17 PROTEIN, ENTEROBACTERIA PHAGE T4; VIRUS PROTEIN;

BACTERIOPHAGE; DNA; ELECTRIC FIELD; HYDROLYSIS; PROTEIN; TRANSLOCATION;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE T4; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA PACKAGING; DNA TRANSLOCATION; DNA TRANSPOSITION; ENERGY; FEEDBACK SYSTEM; FORCE; FREE ENERGY; HYDROLYSIS; INTERACTIONS WITH DNA; MOLECULAR DYNAMICS; MOTOR ACTIVITY; MOTOR PERFORMANCE; NONHUMAN; OPTICAL TWEEZERS; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; STRUCTURE ACTIVITY RELATION; WILD TYPE; BIOLOGICAL MODEL; BIOMECHANICS; CHEMICAL STRUCTURE; CHEMISTRY; ENTEROBACTERIA PHAGE T4; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; BACTERIOPHAGE T4; BIOMECHANICAL PHENOMENA; DNA PACKAGING; HYDROLYSIS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR MOTOR PROTEINS; MUTAGENESIS, SITE-DIRECTED; STATIC ELECTRICITY; VIRAL PROTEINS;

EID: 84902790815     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5173     Document Type: Article

References (56)

1. Smith, D. E. et al. The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature 413, 748-752 (2001). (Pubitemid 33009954)
2. Jardine, P. J. & Anderson, D. L. in: The Bacteriophages. 2nd edn (ed. Calendar, R.) (Oxford University Press, 2006).
3. Feiss, M. & Rao, V. B. in: Viral Molecular Machines (eds Rao, V. & Rossmann, M. G.) 489-509 (Springer, 2012).
4. Morais, M. C. in: Viral Molecular Machines (eds Rao, V. & Rossmann, M. G.) 511-547 (Springer, 2012).
5. Smith, D. E. Single-molecule studies of viral DNA packaging. Curr. Opin. Virol 1, 134 (2011).
6. Chemla, Y. R. & Smith, D. E. in: Viral Molecular Machines (eds Rao, V. & Rossmann, M. G.) 549-584 (Springer, 2012).
7. Tzlil, S., Kindt, J. T., Gelbart, W. M. & Ben-Shaul, A. Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 84, 1616-1627 (2003). (Pubitemid 36322926)
8. Purohit, P. K. et al. Forces during bacteriophage DNA packaging and ejection. Biophys. J. 88, 851-866 (2005). (Pubitemid 40975923)
9. Fuller, D. N. et al. Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi29. Proc. Natl Acad. Sci. USA 104, 11245-11250 (2007). (Pubitemid 47175126)
10. Harvey, S. C., Petrov, A. S., Devkota, B. & Boz, M. B. Viral assembly: a molecular modeling perspective. Phys. Chem. Chem. Phys. 11, 10553-10564 (2009).
11. Berndsen, Z. T., Keller, N., Grimes, S., Jardine, P. J. & Smith, D. E. Nonequilibrium dynamics and ultra-slow relaxation of confined DNA during viral packaging. Proc. Natl Acad. Sci. USA. doi: 10.1073/pnas.1405109111 (2014).
12. Keller, N., delToro, D., Grimes, S., Jardine, P. J. & Smith, D. E. Repulsive DNA-DNA interactions accelerate viral DNA packaging in phage phi29. Phys. Rev. Lett. in press (2014).
13. Fuller, D. N. et al. Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations. J. Mol. Biol. 373, 1113-1122 (2007). (Pubitemid 47542509)
14. Fuller, D. N., Raymer, D. M., Kottadiel, V. I., Rao, V. B. & Smith, D. E. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc. Natl Acad. Sci. USA 104, 16868-16873 (2007). (Pubitemid 350210957)
15. Rickgauer, J. P. et al. Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys. J. 94, 159-167 (2008).
16. Chemla, Y. R. et al. Mechanism of force generation of a viral DNA packaging motor. Cell 122, 683-692 (2005). (Pubitemid 41242634)
17. Moffitt, J. R. et al. Intersubunit coordination in a homomeric ring ATPase. Nature 457, 446-450 (2009).
18. Chistol, G. et al. High degree of coordination and division of labor among subunits in a homomeric ring ATPase. Cell 151, 1017-1028 (2012).
19. Rao, V. B. & Feiss, M. The bacteriophage DNA packaging motor. Annu. Rev. Genet. 42, 647-681 (2008).
20. Mitchell, M. S., Matsuzaki, S., Imai, S. & Rao, V. B. Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals common ATPase center in the large subunit of viral terminases. Nucleic Acids Res. 30 4009-4021 (2002).
21. Iyer, L. M., Leipe, D. D., Koonin, E. V. & Aravind, L. Evolutionary history and higher order classification of AAA\+ ATPases. J. Struct. Biol. 146, 11-31 (2004). (Pubitemid 38369015)
22. Tsay, J. M., Sippy, J., Feiss, M. & Smith, D. E. The Q motif of a viral packaging motor governs its force generation and communicates ATP recognition to DNA interaction. Proc. Natl Acad. Sci. USA 106, 14355-14360 (2009).
23. Tsay, J. M. et al. Mutations altering a structurally conserved loop-helix-loop region of a viral packaging motor change DNA translocation velocity and processivity. J. Biol. Chem. 285, 24282-24289 (2010).
24. Oster, G. & Wang, H. Reverse engineering a protein: the mechanochemistry of ATP synthase. Biochim. Biophys. Acta 1458, 482-510 (2000). (Pubitemid 30320727)
25. Liu, H., Shi, Y., Chen, X. S. & Warshel, A. Simulating the electrostatic guidance of the vectorial translocations in hexameric helicases and translocases. Proc. Natl Acad. Sci. USA 106, 7449-7454 (2009).
26. Mukherjee, S. &Warshel, A. Electrostatic origin of the mechanochemical rotary mechanism and the catalytic dwell of F1-ATPase. Proc. Natl Acad. Sci. USA 108, 20550-20555 (2011).
27. Sun, S. et al. The Structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135, 1251-1262 (2008).
28. Morita, M., Tasaka, M. & Fujisawa, H. Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding. J. Mol. Biol. 245, 635-644 (1995).
29. Dixit, A. B., Ray, K., Thomas, J. A. & Black, L. W. The C-terminal domain of the bacteriophage T4 terminase docks on the prohead portal clip region during DNA packaging. Virology 446, 293-302 (2013).
30. Hegde, S., Padilla-Sanchez, V., Draper, B. & Rao, V. B. Portal-large terminase interactions of the bacteriophage T4 DNA packaging machine implicate a molecular lever mechanism for coupling ATPase to DNA translocation. J. Virol. 86, 4046-4057 (2012).
31. Ray, K., Sabanayagam, C. R., Lakowicz, J. R. & Black, L. W. DNA crunching by a viral packaging motor: compression of a procapsid-portal stalled Y-DNA substrate. Virology 398, 224-232 (2010).
32. Catalano, C. E. (ed.) Viral Genome Packaging Machines: Genetics, Structure, and Mechanism (Kluwer Academic/Plenum Press, 2005).
33. Lebedev, A. A. et al. Structural framework for DNA translocation via the viral portal protein. EMBO J. 26, 1984-1994 (2007). (Pubitemid 46624054)
34. Yu, J., Moffitt, J., Hetherington, C. L., Bustamante, C. & Oster, G. Mechanochemistry of a viral DNA packaging motor. J. Mol. Biol. 400, 186-203 (2010).
35. Serwer, P. & Jiang, W. Dualities in the analysis of phage DNA packaging motors. Bacteriophage 2, 239 (2012).
36. Zhao, H., Christensen, T. E., Kamau, Y. N. & Tang, L. Structures of the phage Sf6 large terminase provide new insights into DNA translocation and cleavage. Proc. Natl Acad. Sci. USA 110, 8075-8080 (2013).
37. Fuller, D. N. et al. A general method for manipulating DNA sequences from any organism with optical tweezers. Nucleic Acids Res. 34, e15 (2006).
38. Keller, D. & Bustamante, C. The mechanochemistry of molecular motors. Biophys. J. 78, 541-556 (2000). (Pubitemid 30211815)
39. Massova, I. & Kollman, P. A. Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect. Drug Discov. Des. 18, 113-135 (2000). (Pubitemid 30191024)
40. Sun, S., Kondabagil, K., Gentz, P. M., Rossmann, M. G. & Rao, V. B. The structure of the ATPase that powers DNA packaging into bacteriophage t4 procapsids. Mol. Cell 25, 943-949 (2007). (Pubitemid 46436529)
41. Singh, N. & Warshel, A. Absolute binding free energy calculations: on the accuracy of computational scoring of protein-ligand interactions. Proteins 78, 1705-1723 (2010).
42. Kottadiel, V. I., Rao, V. B. & Chemla, Y. R. The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4. Proc. Natl Acad. Sci. USA 109, 20000-20005 (2012).
43. Fischer, S., Windshügel, B., Horak, D., Holmes, K. C. & Smith, J. C. Structural mechanism of the recovery stroke in the myosin molecular motor. Proc. Natl Acad. Sci. USA 102, 6873-6878 (2005). (Pubitemid 40675409)
44. Ito, Y., Oroguchi, T. & Ikeguchi, M. Mechanism of the conformational change of the F1-ATPase b subunit revealed by free energy simulations. J. Am. Chem. Soc. 133, 3372-3380 (2011).
45. Allemand, J., Maier, B. & Smith, D. E. Molecular motors for DNA translocation in prokaryotes. Curr. Opin. Biotechnol. 23, 503-509 (2012).
46. Zhang, Z. et al. A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biol. 9, e1000592 (2011).
47. Tao, P. et al. In vitro and in vivo delivery of genes and proteins using the bacteriophage T4 DNA packaging machine. Proc. Natl Acad. Sci. USA 110, 5846-5851 (2013).
48. Kondabagil, K. R., Zhang, Z. & Rao, V. B. The DNA translocating ATPase of bacteriophage T4 packaging motor. J. Mol. Biol. 363, 486-499 (2006).
49. Rickgauer, J. P., Fuller, D. N. & Smith, D. E. DNA as a metrology standard for length and force measurements with optical tweezers. Biophys. J. 91, 4253-4257 (2006). (Pubitemid 44887283)
50. delToro, D. & Smith, D. E. Accurate measurement of force and displacement with optical tweezers using DNA molecules as metrology standards. Appl. Phys. Lett. 104, 143701 (2014).
51. Phillips, J., Isgro, T., Sotomayor, M. & Villa, E. NAMD TUTORIAL. Accessed in June 2013. http://www.ks.uiuc.edu/Training/Tutorials/namd/namd- tutorialhtml.
52. Nelson, M. T. et al. NAMD: a parallel, object-oriented molecular dynamics program. Int. J. High Perform Comput. Appl. 10, 251-268 (1996).
53. MacKerell, A. D., Banavali, N. & Foloppe, N. Development and current status of the CHARMM force field for nucleic acids. Biopolymers 56, 257-265 (2000). (Pubitemid 34105873)
54. Pearlman, D. A. et al. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91, 1-41 (1995).
55. Onufriev, A., Bashford, D. & Case, D. A. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins 55, 383-394 (2004). (Pubitemid 38437495)
56. Karplus, M., Ichiye, T. & Pettitt, B. Configurational entropy of native proteins. Biophys. J. 52, 1083-1085 (1987).