Mechanical operation and intersubunit coordination of ring-shaped molecular motors: Insights from single-molecule studies

Biophysical Journal

Volumn 106, Issue 9, 2014, Pages 1844-1858

  Liu, Shixin ^a,b   Chistol, Gheorghe ^a   Bustamante, Carlos ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR MOTOR; NUCLEOSIDE TRIPHOSPHATASE; PROTEIN SUBUNIT;

BIOMECHANICS; CHEMISTRY; GENETICS; HUMAN; MECHANICS; METABOLISM; PROTEIN SUBUNIT;

BIOMECHANICAL PHENOMENA; HUMANS; MECHANICAL PROCESSES; MOLECULAR MOTOR PROTEINS; NUCLEOSIDE-TRIPHOSPHATASE; PROTEIN SUBUNITS;

EID: 84899876795     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.03.029     Document Type: Review

References (128)

1. C. Bustamante, and Y.R. Chemla D. Izhaky Mechanical processes in biochemistry Annu. Rev. Biochem. 73 2004 705 748
2. A.B. Kolomeisky, and M.E. Fisher Molecular motors: a theorist's perspective Annu. Rev. Phys. Chem. 58 2007 675 695
3. D. Chowdhury Modeling stochastic kinetics of molecular machines at multiple levels: from molecules to modules Biophys. J. 104 2013 2331 2341
4. L.M. Iyer, and D.D. Leipe L. Aravind Evolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 2004 11 31
5. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA+ proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114
6. 1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
7. E.J. Enemark, and L. Joshua-Tor Mechanism of DNA translocation in a replicative hexameric helicase Nature 442 2006 270 275
8. N.D. Thomsen, and J.M. Berger Running in reverse: the structural basis for translocation polarity in hexameric helicases Cell 139 2009 523 534
9. O. Itsathitphaisarn, and R.A. Wing T.A. Steitz The hexameric helicase DnaB adopts a nonplanar conformation during translocation Cell 151 2012 267 277
10. A.N. Kapanidis, and T. Strick Biology, one molecule at a time Trends Biochem. Sci. 34 2009 234 243
11. A.M. van Oijen Honey, I shrunk the DNA: DNA length as a probe for nucleic-acid enzyme activity Biopolymers 85 2007 144 153
12. W.J. Greenleaf, M.T. Woodside, and S.M. Block High-resolution, single-molecule measurements of biomolecular motion Annu. Rev. Biophys. Biomol. Struct. 36 2007 171 190
13. C. Joo, and H. Balci T. Ha Advances in single-molecule fluorescence methods for molecular biology Annu. Rev. Biochem. 77 2008 51 76
14. J.R. Moffitt, and Y.R. Chemla C. Bustamante Recent advances in optical tweezers Annu. Rev. Biochem. 77 2008 205 228
15. I. De Vlaminck, and C. Dekker Recent advances in magnetic tweezers Annu. Rev. Biophys 41 2012 453 472
16. I.J. Finkelstein, and E.C. Greene Supported lipid bilayers and DNA curtains for high-throughput single-molecule studies Methods Mol. Biol. 745 2011 447 461
17. E.M. Puchner, and H.E. Gaub Force and function: probing proteins with AFM-based force spectroscopy Curr. Opin. Struct. Biol. 19 2009 605 614
18. N.G. Walter, and C.-Y. Huang M.A. Sobhy Do-it-yourself guide: how to use the modern single-molecule toolkit Nat. Methods 5 2008 475 489
19. C. Veigel, and C.F. Schmidt Moving into the cell: single-molecule studies of molecular motors in complex environments Nat. Rev. Mol. Cell Biol. 12 2011 163 176
20. T. Ando, T. Uchihashi, and N. Kodera High-speed AFM and applications to biomolecular systems Annu. Rev. Biophys 42 2013 393 414
21. N. Kodera, and D. Yamamoto T. Ando Video imaging of walking myosin V by high-speed atomic force microscopy Nature 468 2010 72 76
22. 1-ATPase Science 333 2011 755 758
23. K. Noi, and D. Yamamoto T. Ogura High-speed atomic force microscopic observation of ATP-dependent rotation of the AAA+ chaperone p97 Structure 21 2013 1992 2002
24. I. Heller, and G. Sitters G.J. Wuite STED nanoscopy combined with optical tweezers reveals protein dynamics on densely covered DNA Nat. Methods 10 2013 910 916
25. M.J. Comstock, T. Ha, and Y.R. Chemla Ultrahigh-resolution optical trap with single-fluorophore sensitivity Nat. Methods 8 2011 335 340
26. X. Long, and J.W. Parks M.D. Stone Mechanical unfolding of human telomere G-quadruplex DNA probed by integrated fluorescence and magnetic tweezers spectroscopy Nucleic Acids Res. 41 2013 2746 2755
27. M.R. Singleton, M.S. Dillingham, and D.B. Wigley Structure and mechanism of helicases and nucleic acid translocases Annu. Rev. Biochem. 76 2007 23 50
28. A.Y. Lyubimov, M. Strycharska, and J.M. Berger The nuts and bolts of ring-translocase structure and mechanism Curr. Opin. Struct. Biol. 21 2011 240 248
29. E.J. Enemark, and L. Joshua-Tor On helicases and other motor proteins Curr. Opin. Struct. Biol. 18 2008 243 257
30. R. Iino, and H. Noji Intersubunit coordination and cooperativity in ring-shaped NTPases Curr. Opin. Struct. Biol. 23 2013 229 234
31. C.L. Hetherington, and J.R. Moffitt C. Bustamante Viral DNA packaging motors Y.E. Goldman, E.M. Ostap, Molecular Motors and Motility 2012 Elsevier Oxford, UK 420 446
32. V.B. Rao, and M. Feiss The bacteriophage DNA packaging motor Annu. Rev. Genet. 42 2008 647 681
33. S.S. Patel, M. Pandey, and D. Nandakumar Dynamic coupling between the motors of DNA replication: hexameric helicase, DNA polymerase, and primase Curr. Opin. Chem. Biol. 15 2011 595 605
34. C. Kaimer, and P.L. Graumann Players between the worlds: multifunctional DNA translocases Curr. Opin. Microbiol. 14 2011 719 725
35. 1-ATPase: how an ATP-driven molecular machine may work Annu. Rev. Biophys. Biomol. Struct. 33 2004 245 268
36. P.D. Boyer The ATP synthase - a splendid molecular machine Annu. Rev. Biochem. 66 1997 717 749
37. T.A. Baker, and R.T. Sauer ClpXP, an ATP-powered unfolding and protein-degradation machine Biochim. Biophys. Acta 1823 2012 15 28
38. O.A. Saleh, and C. Pérals J.-F. Allemand Fast, DNA-sequence independent translocation by FtsK in a single-molecule experiment EMBO J. 23 2004 2430 2439
39. P.J. Pease, and O. Levy N.R. Cozzarelli Sequence-directed DNA translocation by purified FtsK Science 307 2005 586 590
40. J.Y. Lee, and I.J. Finkelstein E.C. Greene Single-molecule imaging of DNA curtains reveals mechanisms of KOPS sequence targeting by the DNA translocase FtsK Proc. Natl. Acad. Sci. USA 109 2012 6531 6536
41. D.E. Smith, and S.J. Tans C. Bustamante The bacteriophage straight φ29 portal motor can package DNA against a large internal force Nature 413 2001 748 752
42. J.P. Rickgauer, and D.N. Fuller D.E. Smith Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage φ29 Biophys. J. 94 2008 159 167
43. D.N. Fuller, and D.M. Raymer D.E. Smith Measurements of single DNA molecule packaging dynamics in bacteriophage λ reveal high forces, high motor processivity, and capsid transformations J. Mol. Biol. 373 2007 1113 1122
44. D.N. Fuller, and D.M. Raymer D.E. Smith Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability Proc. Natl. Acad. Sci. USA 104 2007 16868 16873
45. B. Sun, and D.S. Johnson M.D. Wang ATP-induced helicase slippage reveals highly coordinated subunits Nature 478 2011 132 135
46. H. Yardimci, and A.B. Loveland J.C. Walter Uncoupling of sister replisomes during eukaryotic DNA replication Mol. Cell 40 2010 834 840
47. H. Yardimci, and X. Wang J.C. Walter Bypass of a protein barrier by a replicative DNA helicase Nature 492 2012 205 209
48. E. Delagoutte, and P.H. von Hippel Molecular mechanisms of the functional coupling of the helicase (gp41) and polymerase (gp43) of bacteriophage T4 within the DNA replication fork Biochemistry 40 2001 4459 4477
49. N.M. Stano, and Y.-J. Jeong S.S. Patel DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase Nature 435 2005 370 373
50. M. Pandey, and S. Syed S.S. Patel Coordinating DNA replication by means of priming loop and differential synthesis rate Nature 462 2009 940 943
51. M.-E. Aubin-Tam, and A.O. Olivares M.J. Lang Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine Cell 145 2011 257 267
52. P generates mechanical force to unfold and translocate its protein substrates Cell 145 2011 459 469
53. M. Sen, and R.A. Maillard C. Bustamante The ClpXP protease unfolds substrates using a constant rate of pulling but different gears Cell 155 2013 636 646
54. N. Ribeck, and D.L. Kaplan O.A. Saleh DnaB helicase activity is modulated by DNA geometry and force Biophys. J. 99 2010 2170 2179
55. V.I. Kottadiel, V.B. Rao, and Y.R. Chemla The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4 Proc. Natl. Acad. Sci. USA 109 2012 20000 20005
56. Y.R. Chemla, and K. Aathavan C. Bustamante Mechanism of force generation of a viral DNA packaging motor Cell 122 2005 683 692
57. E. Crozat, and A. Meglio D.J. Sherratt Separating speed and ability to displace roadblocks during DNA translocation by FtsK EMBO J. 29 2010 1423 1433
58. G. Chistol, and S. Liu C. Bustamante High degree of coordination and division of labor among subunits in a homomeric ring ATPase Cell 151 2012 1017 1028
59. S.J. Lee, and S. Syed L. Joshua-Tor Dynamic look at DNA unwinding by a replicative helicase Proc. Natl. Acad. Sci. USA 111 2014 E827 E835
60. S. Bigot, and O.A. Saleh F.-X. Barre Oriented loading of FtsK on KOPS Nat. Struct. Mol. Biol. 13 2006 1026 1028
61. O. Levy, and J.L. Ptacin N.R. Cozzarelli Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase Proc. Natl. Acad. Sci. USA 102 2005 17618 17623
62. J.E. Graham, D.J. Sherratt, and M.D. Szczelkun Sequence-specific assembly of FtsK hexamers establishes directional translocation on DNA Proc. Natl. Acad. Sci. USA 107 2010 20263 20268
63. J.L. Ptacin, and M. Nollmann C. Bustamante Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis Nat. Struct. Mol. Biol. 15 2008 485 493
64. S.R. Barkow, and I. Levchenko R.T. Sauer Polypeptide translocation by the AAA+ ClpXP protease machine Chem. Biol. 16 2009 605 612
65. C. Lee, and M.P. Schwartz A. Matouschek ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal Mol. Cell 7 2001 627 637
66. J.R. Hoskins, and K. Yanagihara S. Wickner ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence Proc. Natl. Acad. Sci. USA 99 2002 11037 11042
67. C. Bustamante, Z. Bryant, and S.B. Smith Ten years of tension: single-molecule DNA mechanics Nature 421 2003 423 427
68. 1-ATPase Nature 427 2004 465 468
69. 1-ATPase single molecules Nature 433 2005 773 777
70. 1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps Cell 93 1998 1117 1124
71. J.R. Moffitt, and Y.R. Chemla C. Bustamante Intersubunit coordination in a homomeric ring ATPase Nature 457 2009 446 450
72. S. Syed, and M. Pandey T. Ha Single-molecule fluorescence reveals the unwinding stepping mechanism of replicative helicase Cell Rep. 6 2014 1037 1045
73. R. Mallik, and B.C. Carter S.P. Gross Cytoplasmic dynein functions as a gear in response to load Nature 427 2004 649 652
74. Liu, S.; G. Chistol,...; C. Bustamante. A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills. Cell. http://dx.doi.org/10.1016/j.cell.2014.02.034.
75. M.D. Wang, and M.J. Schnitzer S.M. Block Force and velocity measured for single molecules of RNA polymerase Science 282 1998 902 907
76. D. Keller, and C. Bustamante The mechanochemistry of molecular motors Biophys. J. 78 2000 541 556
77. G. Oster, and H. Wang Reverse engineering a protein: the mechanochemistry of ATP synthase Biochim. Biophys. Acta 1458 2000 482 510
78. 1-ATPase revealed by single-molecule imaging and manipulation Cell 130 2007 309 321
79. 1-ATPase Nature 410 2001 898 904
80. S.S. Patel, and K.M. Picha Structure and function of hexameric helicases Annu. Rev. Biochem. 69 2000 651 697
81. J.G. Yodh, M. Schlierf, and T. Ha Insight into helicase mechanism and function revealed through single-molecule approaches Q. Rev. Biophys. 43 2010 185 217
82. T.M. Lohman, and K.P. Bjornson Mechanisms of helicase-catalyzed DNA unwinding Annu. Rev. Biochem. 65 1996 169 214
83. M.R. Singleton, and D.B. Wigley Modularity and specialization in superfamily 1 and 2 helicases J. Bacteriol. 184 2002 1819 1826
84. P.H. von Hippel, and E. Delagoutte A general model for nucleic acid helicases and their "coupling" within macromolecular machines Cell 104 2001 177 190
85. M.D. Betterton, and F. Jülicher Opening of nucleic-acid double strands by helicases: active versus passive opening Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71 2005 011904
86. T. Lionnet, and M.M. Spiering V. Croquette Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism Proc. Natl. Acad. Sci. USA 104 2007 19790 19795
87. D.S. Johnson, and L. Bai M.D. Wang Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase Cell 129 2007 1299 1309
88. W. Cheng, and S. Dumont C. Bustamante NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork Proc. Natl. Acad. Sci. USA 104 2007 13954 13959
89. M. Manosas, and X.G. Xi V. Croquette Active and passive mechanisms of helicases Nucleic Acids Res. 38 2010 5518 5526
90. J.L. Adelman, and Y.-J. Jeong S.S. Patel Mechanochemistry of transcription termination factor Rho Mol. Cell 22 2006 611 621
91. S. Sun, and K. Kondabagil V.B. Rao The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces Cell 135 2008 1251 1262
92. D.J. Crampton, S. Mukherjee, and C.C. Richardson DNA-induced switch from independent to sequential dTTP hydrolysis in the bacteriophage T7 DNA helicase Mol. Cell 21 2006 165 174
93. E.J. Mancini, and D.E. Kainov D.I. Stuart Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation Cell 118 2004 743 755
94. T.H. Massey, and C.P. Mercogliano J. Löwe Double-stranded DNA translocation: structure and mechanism of hexameric FtsK Mol. Cell 23 2006 457 469
95. M.R. Singleton, and M.R. Sawaya D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
96. D. Gai, and R. Zhao X.S. Chen Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen Cell 119 2004 47 60
97. A. Martin, T.A. Baker, and R.T. Sauer Rebuilt AAA+ motors reveal operating principles for ATP-fueled machines Nature 437 2005 1115 1120
98. 1-ATPase Nature 386 1997 299 302
99. 1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40° substep rotation Proc. Natl. Acad. Sci. USA 100 2003 14731 14736
100. 1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation Nat. Struct. Mol. Biol. 11 2004 142 148
101. 1-ATPase revealed by catalytic site occupancy during catalysis Biophys. J. 98 2010 1227 1236
102. 1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits Nat. Struct. Mol. Biol. 14 2007 841 846
103. 1-ATPase Proc. Natl. Acad. Sci. USA 110 2013 16468 16473
104. 1-ATPase catalytic cycle follows ADP release Nat. Chem. Biol. 6 2010 814 820
105. 1-ATPase suggested by rotation without 80°/40° substeps of a sluggish mutant at low ATP Biophys. J. 90 2006 1028 1032
106. 1-motor Proc. Natl. Acad. Sci. USA 102 2005 17929 17933
107. +-ATPase/synthase with an essentially drag-free probe Nat. Commun 2 2011 233
108. 1-ATPase J. Biol. Chem. 288 2013 32700 32707
109. I. Donmez, and S.S. Patel Mechanisms of a ring shaped helicase Nucleic Acids Res. 34 2006 4216 4224
110. S.E. Glynn, and A. Martin R.T. Sauer Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine Cell 139 2009 744 756
111. 6 unfoldase: allosteric control of a protein machine Cell 121 2005 1017 1027
112. B.M. Stinson, and A.R. Nager R.T. Sauer Nucleotide binding and conformational switching in the hexameric ring of a AAA+ machine Cell 153 2013 628 639
113. M.S. Strycharska, and E. Arias-Palomo J.M. Berger Nucleotide and partner-protein control of bacterial replicative helicase structure and function Mol. Cell 52 2013 844 854
114. J.M. Tsay, and J. Sippy D.E. Smith 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 2009 14355 14360
115. J.M. Tsay, and J. Sippy D.E. Smith Mutations altering a structurally conserved loop-helix-loop region of a viral packaging motor change DNA translocation velocity and processivity J. Biol. Chem. 285 2010 24282 24289
116. K. Aathavan, and A.T. Politzer C. Bustamante Substrate interactions and promiscuity in a viral DNA packaging motor Nature 461 2009 669 673
117. 1 motor of ATP synthase Nature 396 1998 279 282
118. 1-ATPase rotates in the correct direction Science 319 2008 955 958
119. 1-ATPase plays a significant role in torque production Biophys. J. 95 2008 4837 4844
120. 1-ATPase, the C-terminal end of subunit γ is not required for ATP hydrolysis-driven rotation J. Biol. Chem. 277 2002 23308 23313
121. 1-ATPase devoid of the entire amino-terminal helix of the rotor that fills half of the stator orifice Biophys. J. 101 2011 188 195
122. 1-ATPase: a prototypical rotary molecular motor M.G. Rossmann, V.B. Rao, Viral Molecular Machines 2012 Springer New York 5 16
123. 1-ATP synthase Nat. Struct. Mol. Biol. 11 2004 135 141
124. O. Pänke, and D.A. Cherepanov W. Junge Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme Biophys. J. 81 2001 1220 1233
125. 1-ATPase Nature 459 2009 364 370
126. T.C. Fleming, and J.Y. Shin K. Pogliano Dynamic SpoIIIE assembly mediates septal membrane fission during Bacillus subtilis sporulation Genes Dev. 24 2010 1160 1172
127. J.-B. Fiche, and D.I. Cattoni M. Nöllmann Recruitment, assembly, and molecular architecture of the SpoIIIE DNA pump revealed by superresolution microscopy PLoS Biol. 11 2013 e1001557
128. K.A. Marquis, and B.M. Burton D.Z. Rudner SpoIIIE strips proteins off the DNA during chromosome translocation Genes Dev. 22 2008 1786 1795