Single pore translocation of folded, double-stranded, and tetra-stranded DNA through channel of bacteriophage phi29 DNA packaging motor

Biomaterials

Volumn 53, Issue , 2015, Pages 744-752

  Haque, Farzin ^a,b   Wang, Shaoying ^a,b   Stites, Chris ^c   Chen, Li ^a,b   Wang, Chi ^a,b   Guo, Peixuan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c University of Cincinnati   (United States)

Author keywords

DNA conformation; Electrophysiology; Nanobiotechnology; Nanopore; Phi29 connector; Single channel conductance

Indexed keywords

BACTERIOPHAGES; BIOMIMETICS; CONFORMATIONS; ELECTROPHYSIOLOGY; NANOBIOTECHNOLOGY; NANOPORES;

CROSS SECTIONAL AREA; DNA CONFORMATIONS; DNA-PACKAGING MOTOR; ELECTROPHYSIOLOGICAL PROPERTIES; SINGLE CHANNELS; SINGLE MOLECULE LEVEL; TRANSLOCATION DYNAMICS; TRANSLOCATION PROCESS;

DNA;

DNA; DOUBLE STRANDED DNA; TETRA STRANDED DNA; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; BACILLUS PHAGE PHI29; DNA CONFORMATION; DNA PACKAGING; DNA SEQUENCE; HYDRODYNAMICS; LIPID MEMBRANE; LIPID VESICLE; MACROMOLECULE; NANOPORE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; BACTERIOPHAGE; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BACILLUS PHAGE PHI29;

BACTERIOPHAGES; BIOLOGICAL TRANSPORT; DNA PACKAGING; DNA, VIRAL; NUCLEIC ACID CONFORMATION;

EID: 84927929646     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.104     Document Type: Article

References (71)

1. Neher E., Stevens C.F. Conductance fluctuations and ionic pores in membranes. Annu Rev Biophys Bioeng 1977, 6:345-381.
2. Doyle D.A., Morais C.J., Pfuetzner R.A., Kuo A., Gulbis J.M., Cohen S.L., et al. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 1998, 280(5360):69-77.
3. Hanson P.I., Whiteheart S.W. AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 2005, 6:519-529.
4. Zhao Z., Khisamutdinov E., Schwartz C., Guo P. Mechanism of one-way traffic of hexameric phi29 DNA packaging motor with four electropositive relaying layers facilitating anti-parallel revolution. ACS Nano 2013, 7:4082-4092.
5. Schwartz C., De Donatis G.M., Fang H., Guo P. The ATPase of the phi29 DNA-packaging motor is a member of the hexameric AAA+ superfamily. Virology 2013, 443:20-27.
6. Guo P., Peterson C., Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi29. JMol Biol 1987, 197:229-236.
7. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., et al. Mechanism of force generation of a viral DNA packaging motor. Cell 2005, 122:683-692.
8. Hwang Y., Catalano C.E., Feiss M. Kinetic and mutational dissection of the two ATPase activities of terminase, the DNA packaging enzyme of bacteriophage lambda. Biochemistry 1996, 35:2796-2803.
9. Sabanayagam C.R., Oram M., Lakowicz J.R., Black L.W. Viral DNA packaging studied by fluorescence correlation spectroscopy. Biophys J 2007, 93(4):L17-L19.
10. Meifer W.J.J., Horcajadas J.A., Salas M. Phi29 family of phages. Microbiol Mol Biol Rev 2001, 65(2):261-287.
11. Guo P., Erickson S., Anderson D. Asmall viral RNA is required for invitro packaging of bacteriophage phi29 DNA. Science 1987, 236:690-694.
12. Guo P., Zhang C., Chen C., Trottier M., Garver K. Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol Cell 1998, 2:149-155.
13. Guo P., Lee T.J. Viral nanomotors for packaging of dsDNA and dsRNA. Mol Microbiol 2007, 64:886-903.
14. Sun S., Rao V.B., Rossmann M.G. Genome packaging in viruses. Curr Opin Struct Biol 2010, 20(1):114-120.
15. Simpson A.A., Leiman P.G., Tao Y., He Y., Badasso M.O., Jardine P.J., et al. Structure determination of the head-tail connector of bacteriophage phi29. Acta Cryst 2001, D57:1260-1269.
16. Guasch A., Pous J., Ibarra B., Gomis-Ruth F.X., Valpuesta J.M., Sousa N., et al. Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. JMol Biol 2002, 315(4):663-676.
17. Wendell D., Jing P., Geng J., Subramaniam V., Lee T.J., Montemagno C., et al. Translocation of double-stranded DNA through membrane-adapted phi29 motor protein nanopores. Nat Nanotechnol 2009, 4:765-772.
18. Haque F., Geng J., Montemagno C., Guo P. Incorporation of viral DNA packaging motor channel in lipid bilayers for real-time, single-molecule sensing of chemicals and double-stranded DNA. Nat Protoc 2013, 8:373-392.
19. Jing P., Haque F., Vonderheide A., Montemagno C., Guo P. Robust properties of membrane-embedded connector channel of bacterial virus Phi29 DNA packaging motor. Mol Biosyst 2010, 6:1844-1852.
20. Fang H., Jing P., Haque F., Guo P. Role of channel lysines and "push through a one-way valve" mechanism of viral DNA packaging motor. Biophys J 2012, 102:127-135.
21. Jing P., Haque F., Shu D., Montemagno C., Guo P. One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett 2010, 10:3620-3627.
22. Kasianowicz J.J., Brandin E., Branton D., Deamer D.W. Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci U S A 1996, 93(24):13770-13773.
23. Butler T.Z., Pavlenok M., Derrington I.M., Niederweis M., Gundlach J.H. Single-molecule DNA detection with an engineered MspA protein nanopore. Proc Natl Acad Sci U S A 2008, 105:20647-20652.
24. Geng J., Wang S., Fang H., Guo P. Channel size conversion of Phi29 DNA-packaging nanomotor for discrimination of single- and double-stranded nucleic acids. ACS Nano 2013, 7(4):3315-3323.
25. Geng J., Fang H., Haque F., Zhang L., Guo P. Three reversible and controllable discrete steps of channel gating of a viral DNA packaging motor. Biomaterials 2011, 32:8234-8242.
26. Haque F., Guo P. Membrane-embedded channel of bacteriophage Phi29 DNA-packaging motor for translocation and sensing of double-stranded DNA. Nanopores, sensing and fundamental biological interactions 2011, 77-106. Springer. S.M. Iqbal, R. Bashir (Eds.).
27. Haque F., Lunn J., Fang H., Smithrud D., Guo P. Real-time sensing and discrimination of single chemicals using the channel of Phi29 DNA packaging nanomotor. ACS Nano 2012, 6:3251-3261.
28. Wang S., Haque F., Rychahou P.G., Evers B.M., Guo P. Engineered nanopore of Phi29 DNA-packaging motor for real-time detection of single colon cancer specific antibody in serum. ACS Nano 2013, 7:9814-9822.
29. Ibanez C., Garcia J.A., Carrascosa J.L., Salas M. Overproduction and purification of the connector protein of Bacillus subtilis phage f29. Nucleic Acids Res 1984, 12:2351-2365.
30. Robinson M.A., Wood J.P., Capaldi S.A., Baron A.J., Gell C., Smith D.A., et al. Affinity of molecular interactions in the bacteriophage phi29 DNA packaging motor. Nucleic Acids Res 2006, 34:2698-2709.
31. Guo Y., Blocker F., Xiao F., Guo P. Construction and 3-D computer modeling of connector arrays with tetragonal to decagonal transition induced by pRNA of phi29 DNA-packaging motor. JNanosci Nanotechnol 2005, 5:856-863.
32. Xiao F., Sun J., Coban O., Schoen P., Wang J.C., Cheng R.H., et al. Fabrication of massive sheets of single layer patterned arrays using lipid directed reengineered Phi29 motor dodecamer. ACS Nano 2009, 3:100-107.
33. Cai Y., Xiao F., Guo P. The effect of N- or C-terminal alterations of the connector of bacteriophage phi29 DNA packaging motor on procapsid assembly, pRNA binding, and DNA packaging. Nanomedicine 2008, 4:8-18.
34. Haque F., Li J., Wu H.-C., Liang X.-J., Guo P. Solid-state and biological nanopore for real-time sensing of single chemical and sequencing of DNA. Nano Today 2013, 8:56-74.
35. Branton D., Deamer D.W., Marziali A., Bayley H., Benner S.A., Butler T., et al. The potential and challenges of nanopore sequencing. Nat Biotechnol 2008, 26(10):1146-1153.
36. Venkatesan B.M., Bashir R. Nanopore sensors for nucleic acid analysis. Nat Nanotechnol 2011, 6:615-624.
37. Healy K. Nanopore-based single-molecule DNA analysis. Nanomedicine 2007, 2:459-481.
38. Majd S., Yusko E.C., Billeh Y.N., Macrae M.X., Yang J., Mayer M. Applications of biological pores in nanomedicine, sensing, and nanoelectronics. Curr Opin Biotechnol 2010, 21(4):439-476.
39. Kasianowicz J.J., Robertson J.W., Chan E.R., Reiner J.E., Stanford V.M. Nanoscopic porous sensors. Annu Rev Anal Chem (Palo Alto Calif 2008, 1:737-766.
40. Howorka S., Siwy Z. Nanopore analytics: sensing of single molecules. Chem Soc Rev 2009, 38(8):2360-2384.
41. Reiner J.E., Balijepalli A., Robertson J.W., Campbell J., Suehle J., Kasianowicz J.J. Disease detection and management via single nanopore-based sensors. Chem Rev 2012, 112(12):6431-6451.
42. Li X., Yang X., Qi J., Seeman N. Antiparallel DNA double crossover molecules as components for nanoconstruction. JAm Chem Soc 1996, 118:6131-6140.
43. Henrickson S.E., DiMarzio E.A., Wang Q., Stanford V.M., Kasianowicz J.J. Probing single nanometer-scale pores with polymeric molecular rulers. JChem Phys 2010, 132(13):135101.
44. Li J., Gershow M., Stein D., Brandin E., Golovchenko J.A. DNA molecules and configurations in a solid-state nanopore microscope. Nat Mater 2003, 2:611-615.
45. Balijepalli A., Ettedgui J., Cornio A.T., Robertson J.W., Cheung K.P., Kasianowicz J.J., et al. Quantifying short-lived events in multistate ionic current measurements. ACS Nano 2014, 8(2):1547-1553.
46. Lubensky D.K., Nelson D.R. Driven polymer translocation through a narrow pore. Biophys J 1999, 77(4):1824-1838.
47. Meller A., Nivon L., Branton D. Voltage-driven DNA translocations through a nanopore. Phys Rev Lett 2001, 86(15):3435-3438.
48. Fologea D., Uplinger J., Thomas B., McNabb D.S., Li J. Slowing DNA translocation in a solid-state nanopore. Nano Lett 2005, 5(9):1734-1737.
49. Wanunu M., Sutin J., McNally B., Chow A., Meller A. DNA translocation governed by interactions with solid state nanopores. Biophys J 2008, 95:4716-4725.
50. Meller A., Nivon L., Brandin E., Golovchenko J., Branton D. Rapid nanopore discrimination between single polynucleotide molecules. Proc Natl Acad Sci U S A 2000, 97(3):1079-1084.
51. Robertson J.W.F., Rodrigues C.G., Stanford V.M., Rubinson K.A., Krasilnikov O.V., Kasianowicz J.J. Single-molecule mass spectrometry in solution using a solitary nanopore. Proc Natl Acad Sci U S A 2007, 104(20):8207-8211.
52. Reiner J.E., Kasianowicz J.J., Nablo B.J., Robertson J.W. Theory for polymer analysis using nanopore-based single-molecule mass spectrometry. Proc Natl Acad Sci U S A 2010, 107(27):12080-12085.
53. Balijepalli A., Robertson J.W., Reiner J.E., Kasianowicz J.J., Pastor R.W. Theory of polymer-nanopore interactions refined using molecular dynamics simulations. JAm Chem Soc 2013, 135(18):7064-7072.
54. Storm A.J. Fast DNA translocation through a solid-state nanopore. Nano Lett 2005, 5:1193-1197.
55. Chen L., Conlisk A.T. Forces affecting double-stranded DNA translocation through synthetic nanopores. Biomed Microdevices 2011, 13(2):403-414.
56. Padmanabhan S., Richey B., Anderson C.F., Record M.T. Interaction of an N-methylated polyamine analogue, hexamethonium(2+), with NaDNA: quantitative 14N and 23Na NMR relaxation rate studies of the cation-exchange process. Biochemistry 1988, 27(12):4367-4376.
57. Henrickson S.E., Misakian M., Robertson B., Kasianowicz J.J. Driven DNA transport into an asymmetric nanometer scale pore. Phys Rev Lett 2000, 85:3057-3060.
58. Smith D.E., Perkins T.T., Chu S. Dynamical scaling of DNA diffusion coefficients. Macromolecules 1996, 29(4):1372-1373.
59. Guo P., Schwartz C., Haak J., Zhao Z. Discovery of a new motion mechanism of biomotors similar to the earth revolving around the sun without rotation. Virology 2013, 446:133-143.
60. Baumann C.G., Smith S.B., Bloomfield V.A., Bustamante C. Ionic effects on the elasticity of single DNA molecules. Proc Natl Acad Sci U S A 1997, 94(12):6185-6190.
61. Chen P., Gu J.J., Brandin E., Kim Y.R., Wang Q., Branton D. Probing single DNA molecule transport using fabricated nanopores. Nano Lett 2004, 4:2293-2298.
62. Storm A.J., Chen J.H., Zandbergen H.W., Dekker C. Translocation of double-strand DNA through a silicon oxide nanopore. Phys Rev E 2005, 71(5 Pt 1):051903.
63. Fologea D., Gershow M., Ledden B., McNabb D.S., Golovchenko J.A., Li J. Detecting single stranded DNA with a solid state nanopore. Nano Lett 2005, 5(10):1905-1909.
64. Garaj S., Hubbard W., Reina A., Kong J., Branton D., Golovchenko J.A. Graphene as a subnanometre trans-electrode membrane. Nature 2010, 467(7312):190-193.
65. Merchant C.A., Healy K., Wanunu M., Ray V., Peterman N., Bartel J., et al. DNA translocation through graphene nanopores. Nano Lett 2010, 10(8):2915-2921.
66. Schneider G.F., Kowalczyk S.W., Calado V.E., Pandraud G., Zandbergen H.W., Vandersypen L.M., et al. DNA translocation through graphene nanopores. Nano Lett 2010, 10:3163-3167.
67. 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 2010, 398(2):224-232.
68. Schwartz C., De Donatis G.M., Zhang H., Fang H., Guo P. Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling. Virology 2013, 443:28-39.
69. Guo P., Grainge I., Zhao Z., Vieweger M. Two classes of nucleic acid translocation motors: rotation and revolution without rotation. Cell Biosci 2014, 4(1):54.
70. Guo P. Biophysical studies reveal new evidence for one-way revolution mechanism of bacteriophage phi29 DNA packaging motor. Biophys J 2014, 106(9):1837-1838.
71. De-Donatis G., Zhao Z., Wang S., Huang P.L., Schwartz C., Tsodikov V.O., et al. Finding of widespread viral and bacterial revolution dsDNA translocation motors distinct from rotation motors by channel chirality and size. Cell Biosci 2014, 4:30.