Single-molecule studies of viral DNA packaging

Advances in Experimental Medicine and Biology

Volumn 726, Issue , 2012, Pages 549-584

  Chemla, Yann R ^a   Smith, Douglas E ^b  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CAPSID PROTEIN; MOLECULAR MOTOR; VIRUS DNA;

ARTICLE; BACILLUS PHAGE; BACTERIOPHAGE LAMBDA; BACTERIOPHAGE T4; DNA PACKAGING; DNA PROTEIN COMPLEX; GENE TRANSLOCATION; GENETIC LINKAGE; GENETIC SCREENING; MECHANOTRANSDUCTION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN SUBUNIT; RNA TRANSLATION; STRUCTURAL GENOMICS; STRUCTURE ANALYSIS; THEORETICAL MODEL; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS GENOME; VIRUS REPLICATION;

ADENOSINE TRIPHOSPHATE; BACTERIOPHAGES; DNA PACKAGING; DNA, VIRAL; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; OPTICAL TWEEZERS; PROTEIN CONFORMATION; PROTEIN SUBUNITS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84863275912     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-0980-9_24     Document Type: Article

References (117)

1. Aathavan K, Politzer AT, Kaplan A, Moffi tt JR, Chemla YR, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2009) Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 461:669-673
2. Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM (2005) Direct observation of base-pair stepping by RNA polymerase. Nature 438:460-465 (Pubitemid 41742012)
3. Ali I, Marenduzzo D, Yeomans JM (2006) Polymer packaging and ejection in viral capsids: shape matters. Phys Rev Lett 96:208102
4. Ashkin A (1986) Observation of a single-beam gradient force optical trap for dielectric particles. Opt Lett 11:288-290 (Pubitemid 16117701)
5. Banroques J, Doere M, Dreyfus M, Linder P, Tanner NK (2010) Motif III in superfamily 2 'helicase' helps convert the binding energy of ATP into a high-affi nity RNA binding site in the yeast DEAD-box protein Ded1. J Mol Biol 396:949-966
6. Baumann RG, Black LW (2003) Isolation and characterization of T4 bacteriophage gp17 terminase, a large subunit multimer with enhanced ATPase activity. J Biol Chem 278:4618-4627 (Pubitemid 36800960)
7. Baumann CG, Bloomfi eld VA, Smith SB, Bustamante C, Wang MD, Block SM (2000) Stretching of single collapsed DNA molecules. Biophys J 78:1965-1978 (Pubitemid 30183591)
8. Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61:16-32
9. Black LW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267-292 (Pubitemid 19250048)
10. Burton BM, Marquis KA, Sullivan NL, Rapoport TA, Rudner DZ (2007) The ATPase SpoIIIE transports DNA across fused septal membranes during sporulation in Bacillus subtilis . Cell 131:1301-1312 (Pubitemid 350297414)
11. Bustamante C, Smith SB, Liphardt J, Smith D (2000) Single-molecule studies of DNA mechanics. Curr Opin Struct Biol 10:279-285 (Pubitemid 30333096)
12. Bustamante C, Chemla YR, Forde NR, Izhaky D (2004) Mechanical processes in biochemistry. Annu Rev Biochem 73:705-748 (Pubitemid 39050384)
13. Carter AR, Seol Y, Perkins TT (2009) Precision surface-coupled optical-trapping assay with one-basepair resolution. Biophys J 96:2926-2934
14. Casjens S, Wyckoff E, Hayden M, Sampson L, Eppler K, Randall S, Moreno ET, Serwer P (1992) Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J Mol Biol 224:1055-1074
15. Catalano CE (ed) (2005) Viral genome packaging machines: genetics, structure, and mechanism. Kluwer, New York
16. Cecconi C, Shank EA, Bustamante C, Marqusee S (2005) Direct observation of the three-state folding of a single protein molecule. Science 309:2057-2060 (Pubitemid 41362324)
17. Cerritelli ME, Cheng NQ, Rosenberg AH, McPherson CE, Booy FP, Steven AC (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell 91:271-280 (Pubitemid 27456394)
18. Chemla YR (2010) Revealing the base pair stepping dynamics of nucleic acid motor proteins with optical traps. Phys Chem Chem Phys 12:3080-3095
19. Chemla YR, Aathavan K, Michaelis J, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2005) Mechanism of force generation of a viral DNA packaging motor. Cell 122:683-692 (Pubitemid 41242634)
20. Comolli LR, Spakowitz AJ, Siegerist CE, Jardine PJ, Grimes S, Anderson DL, Bustamante C, Downing KH (2008) Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. Virology 371:267-277 (Pubitemid 351173222)
21. Cordin O, Tanner NK, Doere M, Linder P, Banroques J (2004) The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J 23:2478-2487 (Pubitemid 38988220)
22. Cue D, Feiss M (1997) Genetic evidence that recognition of cosQ the signal for termination of phage lambda DNA packaging, depends on the extent of head fi lling. Genetics 147:7-17 (Pubitemid 27385533)
23. Dokland T, Murialdo H (1993) Structural transitions during maturation of bacteriophage lambda capsids. J Mol Biol 233:682-694 (Pubitemid 23314779)
24. Draper B, Rao VB (2007) An ATP hydrolysis sensor in the DNA packaging motor from bacteriophage T4 suggests an inchworm-type translocation mechanism. J Mol Biol 369:79-94 (Pubitemid 46635439)
25. Duffy C, Feiss M (2002) The large subunit of bacteriophage lambda's terminase plays a role in DNA translocation and packaging termination. J Mol Biol 316:547-561 (Pubitemid 34729240)
26. Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM (2003) Osmotic pressure inhibition of DNA ejection from phage. Proc Natl Acad Sci USA 100:9292-9295 (Pubitemid 37033922)
27. Evilevitch A, Castelnovo M, Knobler CM, Gelbart WM (2004) Measuring the force ejecting DNA from phage. J Phys Chem B 108:6838-6843
28. Evilevitch A, Gober JW, Phillips M, Knobler CM, Gelbart WM (2005) Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. Biophys J 88:751-756 (Pubitemid 40070716)
29. Feiss M & Catalano C (2005) Bacteriophage lambda terminase and the mechanism of viral DNA packaging. in Viral Genome Packaging Machines: Genetics, Structure, and Mechanism', Springer US, pp. 5-39
30. Finer JT, Simmons RM, Spudich JA (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368:113-119 (Pubitemid 24101520)
31. Fokine A, Chipman PR, Leiman PG, Mesyanzhinov VV, Rao VB, Rossmann MG (2004) Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA 101:6003-6008 (Pubitemid 38520518)
32. Forrey C, Muthukumar M (2006) Langevin dynamics simulations of genome packing in bacteriophage. Biophys J 91:25-41 (Pubitemid 44015306)
33. Fujisawa H, Morita M (1997) Phage DNA packaging. Genes Cells 2:537-545 (Pubitemid 127688601)
34. Fuller DN, Gemmen GJ, Rickgauer JP, Dupont A, Millin R, Recouvreux P, Smith DE (2006) A general method for manipulating DNA sequences from any organism with optical tweezers. Nucleic Acids Res 34:e15
35. Fuller DN, Raymer DM, Rickgauer JP, Robertson RM, Catalano CE, Anderson DL, Grimes S, Smith DE (2007a) 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 (Pubitemid 47542509)
36. Fuller DN, Rickgauer JP, Jardine PJ, Grimes S, Anderson DL, Smith DE (2007b) Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi 29. Proc Natl Acad Sci USA 104:11245-11250 (Pubitemid 47175126)
37. Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE (2007c) Single phage T4 DNA packaging motors exhibit barge force generation, high velocity, and dynamic variability. Proc Natl Acad Sci USA 104:16868-16873 (Pubitemid 350210957)
38. Gaussier H, Yang O, Catalano CE (2006) Building a virus from scratch: assembly of an infectious virus using purifi ed components in a rigorously defi ned biochemical assay system. J Mol Biol 357:1154-1166 (Pubitemid 43361922)
39. Gemmen GJ, Millin R, Smith DE (2006) DNA looping by two-site restriction endonucleases: heterogeneous probability distributions for loop size and unbinding force. Nucleic Acids Res 34:2864-2877 (Pubitemid 44540415)
40. Gottesman ME, Weisberg RA (2004) Little lambda, who made thee? Microbiol Mol Biol Rev 68:796-813 (Pubitemid 39628537)
41. Grayson P, Evilevitch A, Inamdar MM, Purohit PK, Gelbart WM, Knobler CM, Phillips R (2006) The effect of genome length on ejection forces in bacteriophage lambda. Virology 348:430-436
42. Grayson P, Han L, Winther T, Phillips R (2007) Real-time observations of single bacteriophage lambda DNA ejections in vitro. Proc Natl Acad Sci USA 104:14652-14657 (Pubitemid 350003198)
43. Greenleaf WJ, Woodside MT, Block SM (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu Rev Biophys Biomol Struct 36:171-190 (Pubitemid 46998115)
44. Grimes S, Anderson D (1989) In vitro packaging of bacteriophage phi 29 DNA restriction fragments and the role of the terminal protein gp3. J Mol Biol 209:91-100 (Pubitemid 19237809)
45. Grimes S, Anderson D (1997) The bacteriophage phi29 packaging proteins supercoil the DNA ends. J Mol Biol 266:901-914 (Pubitemid 27122597)
46. Grimes S, Jardine PJ, Anderson D (2002) Bacteriophage phi 29 DNA packaging. Adv Virus Res 58:255-294
47. Guasch A, Pous J, Ibarra B, Gomis-Ruth FX, Valpuesta JM, Sousa N, Carrascosa JL, Coll M (2002) Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J Mol Biol 315:663-676 (Pubitemid 34729317)
48. Guo P, Peterson C, Anderson D (1987) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J Mol Biol 197:229-236
49. Hang JQ, Tack BF, Feiss M (2000) ATPase center of bacteriophage lambda terminase involved in post-cleavage stages of DNA packaging: identifi cation of ATP-interactive amino acids. J Mol Biol 302:777-795
50. Harvey SC, Petrov AS, Devkota B, Boz MB (2009) Viral assembly: a molecular modeling perspective. Phys Chem Chem Phys 11:10553-10564
51. Hendrix RW (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 75:4779-4783 (Pubitemid 9048617)
52. Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S, Walter JM, Falk W, Anderson DL, Bustamante C (2007) Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol 5:e59
53. Joo C, Balci H, Ishitsuka Y, Buranachai C, Ha T (2008) Advances in single-molecule fl uorescence methods for molecular biology. Annu Rev Biochem 77:51-76
54. Kindt J, Tzlil S, Ben-Shaul A, Gelbart WM (2001) DNA packaging and ejection forces in bacteriophage. Proc Natl Acad Sci USA 98:13671-13674 (Pubitemid 33115956)
55. Kondabagil KR, Zhang Z, Rao VB (2006) The DNA translocating ATPase of bacteriophage T4 packaging motor. J Mol Biol 363:486-499
56. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, Poliakov A, Potter CS, Carragher B, Johnson JE (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312: 1791-1795 (Pubitemid 43962896)
57. Lander GC, Evilevitch A, Jeembaeva M, Potter CS, Carragher B, Johnson JE (2008) Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM. Structure 16:1399-1406
58. Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984-1994 (Pubitemid 46624054)
59. Lehninger AL, Nelson DL, Cox MM (1993) Principles of biochemistry. Worth Publishers, New York
60. Lisal J, Lam TT, Kainov DE, Emmett MR, Marshall AG, Tuma R (2005) Functional visualization of viral molecular motor by hydrogen-deuterium exchange reveals transient states. Nat Struct Mol Biol 12:460-466 (Pubitemid 43085908)
61. Lu HP, Xun L, Xie XS (1998) Single-molecule enzymatic dynamics. Science 282:1877-1882 (Pubitemid 28555264)
62. Maluf NK, Gaussier H, Bogner E, Feiss M, Catalano CE (2006) Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry (N Y) 45:15259-15268 (Pubitemid 46032453)
63. Mangenot S, Hochrein M, Radler J, Letellier L (2005) Real-time imaging of DNA ejection from single phage particles. Curr Biol 15:430-435 (Pubitemid 40323528)
64. Manning GS (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys 11:179-246 (Pubitemid 8373665)
65. Marenduzzo D, Micheletti C (2003) Thermodynamics of DNA packaging inside a viral capsid: the role of DNA intrinsic thickness. J Mol Biol 330:485-492 (Pubitemid 36808682)
66. Michaelis J, Muschielok A, Andrecka J, Kugel W, Moffi tt JR (2009) DNA based molecular motors. Phys Life Rev 6:250-255
67. Mitchell MS, Rao VB (2004) Novel and deviant Walker A ATP-binding motifs in bacteriophage large terminase-DNA packaging proteins. Virology 321:217-221 (Pubitemid 38406036)
68. Mitchell MS, Matsuzaki S, Imai S, Rao VB (2002) Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases. Nucleic Acids Res 30:4009-4021
69. Moffitt JR, Chemla YR, Izhaky D, Bustamante C (2006) Differential detection of dual traps improves the spatial resolution of optical tweezers. Proc Natl Acad Sci USA 103:9006-9011 (Pubitemid 43902524)
70. Moffi tt JR, Chemla YR, Smith SB, Bustamante C (2008) Recent advances in optical tweezers. Annu Rev Biochem 77:205-228
71. Moffi tt JR, Chemla YR, Aathavan K, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2009) Intersubunit coordination in a homomeric ring ATPase. Nature 457:446-450
72. Moffi tt JR, Chemla YR, Bustamante C (2010) Mechanistic constraints from the substrate concentration dependence of enzymatic fl uctuations. Proc Natl Acad Sci USA 107:15739-15744
73. Morais MC, Choi KH, Koti JS, Chipman PR, Anderson DL, Rossmann MG (2005) Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol Cell 18:149-159
74. Morais MC, Koti JS, Bowman VD, Reyes-Aldrete E, Anderson DL, Rossmann MG (2008) Defi ning molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure 16:1267-1274
75. Morita M, Tasaka M, Fujisawa H (1993) DNA packaging ATPase of bacteriophage T3. Virology 193:748-752
76. Mosig G, Eiserling F (2006) T4 and related phages: structure and development. In: Calendar R, Abedon ST (eds) The bacteriophages. Oxford University Press, Oxford
77. Murialdo H (1991) Bacteriophage lambda DNA maturation and packaging. Annu Rev Biochem 60:125-153
78. Myong S, Stevens BC, Ha T (2006) Bridging conformational dynamics and function using single-molecule spectroscopy. Structure 14:633-643
79. Neuman KC, Block SM (2004) Optical trapping. Rev Sci Instrum 75:2787-2809
80. Neuman KC, Nagy A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 5:491-505 (Pubitemid 351761756)
81. Odijk T (1998) Hexagonally packed DNA within bacteriophage T7 stabilized by curvature stress. Biophys J 75:1223-1227 (Pubitemid 28397592)
82. Oram M, Sabanayagam C, Black LW (2008) Modulation of the packaging reaction of bacteriophage t4 terminase by DNA structure. J Mol Biol 381:61-72
83. Oster G, Wang H (2000) Reverse engineering a protein: the mechanochemistry of ATP synthase. Biochim Biophys Acta 1458:482-510 (Pubitemid 30320727)
84. Oster G, Wang H (2003) Rotary protein motors. Trends Cell Biol 13:114-121 (Pubitemid 36293783)
85. Perkins TT, Li HW, Dalal RV, Gelles J, Block SM (2004) Forward and reverse motion of single RecBCD molecules on DNA. Biophys J 86:1640-1648 (Pubitemid 38295598)
86. Perucchetti R, Parris W, Becker A, Gold M (1988) Late stages in bacteriophage lambda head morphogenesis: in vitro studies on the action of the bacteriophage lambda D-gene and W-gene products. Virology 165:103-114
87. Purohit PK, Kondev J, Phillips R (2003) Mechanics of DNA packaging in viruses. Proc Natl Acad Sci USA 100:3173-3178 (Pubitemid 36356558)
88. Purohit PK, Inamdar MM, Grayson PD, Squires TM, Kondev J, Phillips R (2005) Forces during bacteriophage DNA packaging and ejection. Biophys J 88:851-866 (Pubitemid 40975923)
89. Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647-681
90. Rau DC, Parsegian VA (1992) Direct measurement of the intermolecular forces between counterion-condensed DNA double helices - evidence for long-range attractive hydration forces. Biophys J 61:246-259
91. Ray K, Ma J, Oram M, Lakowicz JR, Black LW (2010a) Single-molecule and FRET fl uorescence correlation spectroscopy analyses of phage DNA packaging: colocalization of packaged phage T4 DNA ends within the capsid. J Mol Biol 395:1102-1113
92. Ray K, Sabanayagam CR, Lakowicz JR, Black LW (2010b) DNA crunching by a viral packaging motor: compression of a procapsid-portal stalled Y-DNA substrate. Virology 398:224-232
93. Rickgauer, JP and Smith, DE (2008) Single-Molecule Studies of DNA: Visualization and Manipulation of Individual DNA Molecules with Fluorescence Microscopy and Optical Tweezers. In: Borsali R and Pecora R (ed) Soft Matter: Scattering, Imaging and Manipulation, Vol. 4, Springer
94. Rickgauer JP, Fuller DN, Smith DE (2006) DNA as a metrology standard for length and force measurements with optical tweezers. Biophys J 91:4253-4257
95. Rickgauer JP, Fuller DN, Grimes S, Jardine PJ, Anderson DL, Smith DE (2008) Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys J 94:159-167
96. Riemer SC, Bloomfi eld VA (1978) Packaging of DNA in bacteriophage heads - some considerations on energetics. Biopolymers 17:785-794 (Pubitemid 8310589)
97. Robertson RM, Laib S, Smith DE (2006) Diffusion of isolated DNA molecules: dependence on length and topology. Proc Natl Acad Sci USA 103:7310-7314 (Pubitemid 43727829)
98. Ross JL, Ali MY, Warshaw DM (2008) Cargo transport: molecular motors navigate a complex cytoskeleton. Curr Opin Cell Biol 20:41-47
99. Sabanayagam CR, Oram M, Lakowicz JR, Black LW (2007) Viral DNA packaging studied by fl uorescence correlation spectroscopy. Biophys J 93:L17-L19 (Pubitemid 47330887)
100. Shu D, Zhang H, Jin J, Guo P (2007) Counting of six pRNAs of phi29 DNA-packaging motor with customized singlemolecule dual-view system. EMBO J 26:527-537 (Pubitemid 46160952)
101. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS, Rossmann MG (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408:745-750 (Pubitemid 32015993)
102. Sippy J, Feiss M (2004) Initial cos cleavage of bacteriophage lambda concatemers requires proheads and gpFI in vivo. Mol Microbiol 52:501-513 (Pubitemid 38520718)
103. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage phi29 portal motor can package DNA against a large internal force. Nature 413:748-752 (Pubitemid 33009954)
104. Smith SB, Cui Y, Bustamante C (2003) Optical-trap force transducer that operates by direct measurement of light momentum. Methods Enzymol 361:134
105. Spakowitz AJ, Wang ZG (2005) DNA packaging in bacteriophage: is twist important? Biophys J 88:3912-3923 (Pubitemid 40991104)
106. Sternberg N, Weisberg R (1977) Packaging of coliphage lambda DNA. II. The role of the gene D protein. J Mol Biol 117:733-759 (Pubitemid 8256701)
107. Sun S, Kondabagil K, Gentz PM, Rossmann MG, Rao VB (2007) The structure of the ATPase that powers DNA packaging into bacteriophage t4 procapsids. Mol Cell 25:943-949 (Pubitemid 46436529)
108. Sun S, Kondabagil K, Draper B, Alam TI, Bowman VD, Zhang Z, Hegde S, Fokine A, Rossmann MG, Rao VB (2008) The structure of the Phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135:1251-1262
109. Tinoco I Jr, Li PT, Bustamante C (2006) Determination of thermodynamics and kinetics of RNA reactions by force. Q Rev Biophys 39:325-360 (Pubitemid 44950379)
110. Tsay JM, Sippy J, Feiss M, Smith DE (2009) 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
111. Tsay JM, Sippy J, DelToro D, Andrews BT, Draper B, Rao V, Catalano CE, Feiss M, Smith DE (2010) 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
112. Tzlil S, Kindt JT, Gelbart WM, Ben-Shaul A (2003) Forces and pressures in DNA packaging and release from viral capsids. Biophys J 84:1616-1627 (Pubitemid 36322926)
113. van Oijen AM, Blainey PC, Crampton DJ, Richardson CC, Ellenberger T, Xie XS (2003) Single-molecule kinetics of lambda exonuclease reveal base dependence and dynamic disorder. Science 301:1235-1238 (Pubitemid 37052212)
114. Wang MD, Schnitzer MJ, Yin H, Landick R, Gelles J, Block SM (1998) Force and velocity measured for single molecules of RNA polymerase. Science 282:902-907 (Pubitemid 28507515)
115. Xue Q, Yeung ES (1995) Differences in the chemical reactivity of individual molecules of an enzyme. Nature 373:681-683
116. Yang Q, Catalano CE (2003) Biochemical characterization of bacteriophage lambda genome packaging in vitro. Virology 305:276-287 (Pubitemid 36259662)
117. Yang Q, Maluf NK, Catalano CE (2008) Packaging of a unit-length viral genome: the role of nucleotides and the gpD decoration protein in stable nucleocapsid assembly in bacteriophage lambda. J Mol Biol 383:1037-1048