Distinguishing Inchworm and Hand-Over-Hand Processive Kinesin Movement by Neck Rotation Measurements
Abstract
The motor enzyme kinesin makes hundreds of unidirectional 8-nanometer steps without detaching from or freely sliding along the microtubule on which it moves. We investigated the kinesin stepping mechanism by immobilizing a Drosophila kinesin derivative through the carboxyl-terminal end of the neck coiled-coil domain and measuring orientations of microtubules moved by single enzyme molecules at submicromolar adenosine triphosphate concentrations. The kinesin-mediated microtubule-surface linkage was sufficiently torsionally stiff (>/=2.0 +/- 0.9 x 10(-20) Newton meters per radian2) that stepping by the hypothesized symmetric hand-over-hand mechanism would produce 180 degree rotations of the microtubule relative to the immobilized kinesin neck. In fact, there were no rotations, a finding that is inconsistent with symmetric hand-over-hand movement. An alternative "inchworm" mechanism is consistent with our experimental results.
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In the inchworm model, the leading motor is always leading, the trailing motor is always trailing, and one motor remains enzymatically inactive throughout a processive run.
“In this model, the leading motor is always leading, the trailing motor is always trailing, and one motor remains enzymatically inactive throughout a processive run.”
From Stepping and Stretching (2003) · cites this paper as [33]
Cites
Direct observation of kinesin stepping by optical trapping interferometry
Svoboda, K., Schmidt, C. F., Schnapp, B. J., & Block, S. M. (1993) · Nature · doi:10.1038/365721a0 · Cited by 1,910 · see citing works
The Crystal Structure of Dimeric Kinesin and Implications for Microtubule-Dependent Motility
Kozielski, F., Sack, S., Marx, A., Thormählen, M., Schönbrunn, E., Biou, V, Thompson, A., Mandelkow, E.-M., & Mandelkow, E. (1997) · Cell · doi:10.1016/s0092-8674(00)80489-4 · Cited by 408 · see citing works
Coupling of kinesin steps to ATP hydrolysis
Hua, W., Young, E. C., Fleming, M. L., & Gelles, J. (1997) · Nature · doi:10.1038/41118 · Cited by 358 · see citing works
Self-citationEvidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis.
Hackney, D. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.6865 · Cited by 351 · see citing works
Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains
Hackney, D. D. (1995) · Nature · doi:10.1038/377448a0 · Cited by 177 · see citing works
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Myosin V Walks Hand-Over-Hand: Single Fluorophore Imaging with 1.5-nm Localization
Yildiz, A., Forkey, J., McKinney, S., Ha, T., Goldman, Y., & Selvin, P. (2003) · Science · doi:10.1126/science.1084398 · Cited by 1,870 · see citing works
Yildiz, A., Tomishige, M., Vale, R. D., & Selvin, P. R. (2004) · Science · doi:10.1126/science.1093753 · Cited by 965 · see citing works
Video imaging of walking myosin V by high-speed atomic force microscopy
Kodera, N., Yamamoto, D., Ishikawa, R., & Ando, T. (2010) · Nature · doi:10.1038/nature09450 · Cited by 836 · see citing works
Single-molecule analysis of dynein processivity and stepping behavior.
Reck-Peterson, S., Yildiz, A., Carter, A., Gennerich, A., Zhang, N., & Vale, R. (2006) · Cell · doi:10.1016/j.cell.2006.05.046 · Cited by 649 · see citing works
“In the second model (‘‘asymmetric inchworm’’) (Hua et al., 2002), a single head always takes the leading position, extending forward to a new binding site while the rear head remains stationary, and then the rear head catches up in the next cycle (Figure S11).”
BackgroundIntracellular Transport and Kinesin Superfamily Proteins, KIFs: Structure, Function, and Dynamics
Hirokawa, N., & Noda, Y. (2008) · Physiological Reviews · doi:10.1152/physrev.00023.2007 · Cited by 510 · see citing works
Kinesin Moves by an Asymmetric Hand-Over-Hand Mechanism
Asbury, C. L., Fehr, A. N., & Block, S. M. (2003) · Science · doi:10.1126/science.1092985 · Cited by 511 · see citing works
Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization
Forkey, J., Quinlan, M., Shaw, M., Corrie, J., & Goldman, Y. (2003) · Nature · doi:10.1038/nature01529 · Cited by 450 · see citing works
Force-Induced Bidirectional Stepping of Cytoplasmic Dynein
Gennerich, A., Carter, A. P., Reck‐Peterson, S. L., & Vale, R. D. (2007) · Cell · doi:10.1016/j.cell.2007.10.016 · Cited by 376 · see citing works
“…explained by the trailing head passing the leading head and landing on various possible binding sites, although 4 nm steps might be best explained by an inchworm-like progression (Hua et al., 2002) in which the heads do not pass one another (see Figure S16 for models of differently sized stepping).”
BackgroundFilming Biomolecular Processes by High-Speed Atomic Force Microscopy
Ando, T., Uchihashi, T., & Simon Scheuring, A. (2014) · Chemical Reviews · doi:10.1021/cr4003837 · Cited by 398 · see citing works
Fluorescence Imaging with One Nanometer Accuracy: Application to Molecular Motors
Yıldız, A., & Selvin, P. R. (2005) · Accounts of Chemical Research · doi:10.1021/ar040136s · Cited by 322 · see citing works
Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein
Toba, S., Watanabe, T. M., Yamaguchi, L., Toyoshima, Y. Y., & Higuchi, H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508511103 · Cited by 327 · see citing works
Kinesin Motor Mechanics: Binding, Stepping, Tracking, Gating, and Limping
Block, S. M. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.100677 · Cited by 338 · see citing works
“At least four single‐molecule experiments bear directly on this question (Hua et al., 2002; Asbury et al., 2003; Kaseda et al., 2003; Yildiz et al., 2004).”
BackgroundResultInfluentialRosenfeld, S. S., Fordyce, P. M., Jefferson, G. M., King, P. H., & Block, S. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300849200 · Cited by 188 · see citing works
Single-molecule assay reveals strand switching and enhanced processivity of UvrD.
Dessinges, M., Lionnet, T., Xi, X.-G., Bensimon, D., & Croquette, V. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0306713101 · Cited by 188 · see citing works
High-Speed Atomic Force Microscopy
Ando, T., Uchihashi, T., & Kodera, N. (2012) · Japanese Journal of Applied Physics · doi:10.1143/jjap.51.08ka02 · Cited by 40 · see citing works
Alternate fast and slow stepping of a heterodimeric kinesin molecule
Kaseda, K., Higuchi, H., & Hirose, K. (2003) · Nature Cell Biology · doi:10.1038/ncb1067 · Cited by 179 · see citing works
“In contrast, there are other models in which one of the heads is always leading; for example, the 'inchworm' mode”
ResultMolecular machines working on surfaces and at interfaces.
Balzani, V., Credi, A., & Venturi, M. (2008) · ChemPhysChem · doi:10.1002/cphc.200700528 · Cited by 167 · see citing works
Processivity of the single-headed kinesin KIF1A through biased binding to tubulin
Okada, Y., Higuchi, H., & Hirokawa, N. (2003) · Nature · doi:10.1038/nature01804 · Cited by 196 · see citing works
“This dimeric structure poses a barrier to solving its mechanis”
BackgroundForce Generation in Kinesin Hinges on Cover-Neck Bundle Formation
Hwang, W., Lang, M. J., & Karplus, M. (2008) · Structure · doi:10.1016/j.str.2007.11.008 · Cited by 161 · see citing works
“Conventional kinesin walks to the plus end of MT and is believed to walk by an asymmetric hand-over-hand mode, although the mechanism is not well understood (Hua et al., 2002; Asbury et al., 2003; Yildiz et al., 2004; Kaseda et al., 2003).”
MINFLUX dissects the unimpeded walking of kinesin-1
Wirth, J. O., Scheiderer, L., Engelhardt, T., Engelhardt, J., Matthias, J., & Hell, S. W. (2023) · Science · doi:10.1126/science.ade2650 · Cited by 186 · see citing works
“4 symmetric or asymmetric is still debated (24-26).”
BackgroundSINGLE-MOLECULE FLUORESCENCE SPECTROSCOPY AND MICROSCOPY OF BIOMOLECULAR MOTORS
Peterman, E. J. G., Sosa, H., & Moerner, W. E. (2004) · Annual Review of Physical Chemistry · doi:10.1146/annurev.physchem.55.091602.094340 · Cited by 158 · see citing works
Myosin V is a left-handed spiral motor on the right-handed actin helix
Ali, M. Y., Uemura, S., Adachi, K., Itoh, H., Kinosita, K., & Ishiwata, S. (2002) · Nature Structural Biology · doi:10.1038/nsb803 · Cited by 152 · see citing works
Detection of fractional steps in cargo movement by the collective operation of kinesin-1 motors
Leduc, C., Ruhnow, F., Howard, J., & Diez, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701864104 · Cited by 134 · see citing works
Thermodynamic properties of the kinesin neck-region docking to the catalytic core.
Rice, S. E., Cui, Y., Sindelar, C., Naber, N., Matuska, M., Vale, R., & Cooke, R. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74992-3 · Cited by 140 · see citing works
“Recent experiments have suggested that kinesin may not move by this type of mechanism and instead might ‘‘inchworm’’ along the microtubule or move by an asymmetric hand-over-hand mechanism (Hua et al., 2002).”
BackgroundDirect observation of intermediate states during the stepping motion of kinesin-1
Isojima, H., Iino, R., Niitani, Y., Noji, H., & Tomishige, M. (2016) · Nature Chemical Biology · doi:10.1038/nchembio.2028 · Cited by 141 · see citing works
Single-molecule observations of neck linker conformational changes in the kinesin motor protein
Tomishige, M., Stuurman, N., & Vale, R. D. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1151 · Cited by 109 · see citing works
“As a control, two dyes were placed within the catalytic core itself (28-149), and no nucleotide-dependent change in smFRET efficiency was observed (Fig.”
Inhibition of kinesin motility by ADP and phosphate supports a hand-over-hand mechanism
Schief, W. R., Clark, R. H., Crevenna, A. H., & Howard, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0304369101 · Cited by 119 · see citing works
Kinesin: world's tiniest biped
Asbury, C. L. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.12.002 · Cited by 116 · see citing works
The physical chemistry of mechanoresponsive polymers
Kucharski, T. J., & Boulatov, R. (2011) · Journal of Materials Chemistry · doi:10.1039/c0jm04079g · Cited by 129 · see citing works
Klumpp, L. M., Hoenger, A., & Gilbert, S. P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307691101 · Cited by 107 · see citing works
Bacteriophage T7 DNA ejection into cells is initiated by an enzyme‐like mechanism
Kemp, P., Gupta, M., & Molineux, I. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04204.x · Cited by 104 · see citing works
“This speculative model for DNA translocation by gp16 uses as an analogy the mechanism of kinesin movement along microtubules (Hua et al., 2002; Asbury et al., 2003).”
BackgroundBao, G. (2002) · Journal of the Mechanics and Physics of Solids · doi:10.1016/s0022-5096(02)00035-2 · Cited by 112 · see citing works
“However, as revealed by recent experimental evidence, such rotation does not occur during kinesin movement (Hua et al., 2002).”
BackgroundSnyder, G. E., Sakamoto, T., Hammer, J., Sellers, J., & Selvin, P. (2004) · Biophysical Journal · doi:10.1529/biophysj.103.036897 · Cited by 99 · see citing works
“This is in contrast to an inchworm model, which has, for example, been postulated for kinesin (Hua et al., 2002).”
ResultMicroscopic evidence for a minus‐end‐directed power stroke in the kinesin motor ncd
Wendt, T., Volkmann, N., Skiniotis, G., Goldie, K., Müller, J., Mandelkow, E., & Hoenger, A. (2002) · EMBO Journal · doi:10.1093/emboj/cdf622 · Cited by 98 · see citing works
‘Life is motion’: multiscale motility of molecular motors
Lipowsky, R., & Klumpp, S. (2005) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2004.12.034 · Cited by 105 · see citing works
“[27].”
Xiao, L., Qiao, Y., He, Y., & Yeung, E. S. (2011) · Journal of the American Chemical Society · doi:10.1021/ja203289m · Cited by 95
Myosin at work: Motor adaptations for a variety of cellular functions
O’Connell, C. B., Tyska, M. J., & Mooseker, M. S. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.06.012 · Cited by 101 · see citing works
“The inchworm model, put forth to explain the movement of kinesin [121], argues that the relative position of the heads (i.”
BackgroundKinesin: walking, crawling or sliding along?
YILDIZ, A., & Selvin, P. R. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2004.12.007 · Cited by 86 · see citing works
Kinesin rotates unidirectionally and generates torque while walking on microtubules
Ramaiya, A., Roy, B., Bugiel, M., & Schäffer, E. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706985114 · Cited by 98 · see citing works
“However, experiments done at low ATP concentrations only revealed occasional, random motor rotations (9, 10).”
BackgroundResultVale, R. (2003) · Journal of Cell Biology · doi:10.1083/jcb.200308093 · Cited by 89 · see citing works
“In contrast, electron microscopic images of myosin V bound to actin instantly revealed a wealth of information on the conformational states of the lever arm.”
BackgroundSingle-Molecule Biology: What Is It and How Does It Work?
Zlatanova, J. S., & Holde, K. V. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.10.017 · Cited by 93 · see citing works
Single Molecule Fluorescence Approaches Shed Light on Intracellular RNAs
Pitchiaya, S., Heinicke, L. A., Custer, T. C., & Walter, N. G. (2014) · Chemical Reviews · doi:10.1021/cr400496q · Cited by 80 · see citing works
The mitotic kinesin CENP-E is a processive transport motor
Yardimci, H., van Duffelen, M., Mao, Y., Rosenfeld, S. S., & Selvin, P. R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711314105 · Cited by 72 · see citing works
“Two models have been proposed to explain the stepping mechanism of molecular motors: ‘‘inchworm’’ and ‘‘hand-over-hand’’ (12, 14).”
BackgroundNucleotide‐induced conformations in the neck region of dimeric kinesin
Skiniotis, G., Surrey, T., Altmann, S., Gross, H., Song, Y.-H., Mandelkow, E., & Hoenger, A. (2003) · EMBO Journal · doi:10.1093/emboj/cdg164 · Cited by 79 · see citing works
“double-bound con®guration partially explains the alternating head catalysis mechanism in kinesin, which seems to be a key element for processive movement (Cross, 1995; Hua et al., 2002).”
Dissecting the Kinematics of the Kinesin Step
Zhang, Z., & Thirumalai, D. (2012) · Structure · doi:10.1016/j.str.2012.02.013 · Cited by 72 · see citing works
Design, Synthesis, and Operation of Small Molecules That Walk along Tracks
von Delius, M., Geertsema, E. M., Leigh, D. A., & Tang, D. D. (2010) · Journal of the American Chemical Society · doi:10.1021/ja106486b · Cited by 84 · see citing works
Complex formation with kinesin motor domains affects the structure of microtubules.
Krebs, A., Goldie, K., & Hoenger, A. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.10.039 · Cited by 71 · see citing works
A mobile kinesin-head intermediate during the ATP-waiting state
Asenjo, A. B., & Sosa, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808355106 · Cited by 64 · see citing works
Single-molecule fluorescence to study molecular motors
Park, H., Toprak, E., & Selvin, P. R. (2007) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583507004611 · Cited by 71 · see citing works
“Hua and colleagues measured the rotation of microtubules by single kinesin using a microtubule gliding assay, and did not observe 180x rotation of the microtubules (Hua et al. 2002).”
BackgroundUnconstrained Steps of Myosin VI Appear Longest among Known Molecular Motors
Ali, M. Y., Homma, K., Iwane, A. H., Adachi, K., Itoh, H., Kinosita, K., Yanagida, T., & Ikebe, M. (2004) · Biophysical Journal · doi:10.1529/biophysj.103.037416 · Cited by 58 · see citing works
“Also, as with kinesin (Hua et al., 2002) and myosin V (Ali et al., 2002), we did not observe clear 180 rotation of myosin VI around its own axis that is expected to accompany every step if a motor with two identical heads attains the same posture after each step (Howard, 1996).”
BackgroundNath, S. (2008) · International Journal of Molecular Sciences · doi:10.3390/ijms9091784 · Cited by 57 · see citing works
“However, experimental data from the Gelles group contradicted the above because the postulated 180 swiveling or rotation was not observed with each step [64].”
BackgroundResultInfluentialEnergy transfer from adenosine triphosphate: quantitative analysis and mechanistic insights.
Nath, S. S., & Nath, S. (2009) · Journal of Physical Chemistry B · doi:10.1021/jp809678n · Cited by 55 · see citing works
Measuring Kinesin's First Step
Rosenfeld, S. S., Xing, J., Jefferson, G. M., Cheung, H. C., & King, P. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205261200 · Cited by 54 · see citing works
Label-free Imaging of Microtubules with Sub-nm Precision Using Interferometric Scattering Microscopy
Andrecka, J., Arroyo, J. O., Lewis, K. D., Cross, R. A., & Kukura, P. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2015.10.055 · Cited by 55 · see citing works
An optical apparatus for rotation and trapping
Gutiérrez-Medina, B., Andreasson, J. O. L., Greenleaf, W., Laporta, A., & Block, S. (2010) · Methods in Enzymology · doi:10.1016/s0076-6879(10)75015-1 · Cited by 54
“Finally, mechanoenzymes that translocate along linear polymers, such as myosin or kinesin, may also generate (or respond to) torque (Hua et al., 2002).”
Processive and Nonprocessive Models of Kinesin Movement
Endow, S. A., & Barker, D. S. (2003) · Annual Review of Physiology · doi:10.1146/annurev.physiol.65.092101.142550 · Cited by 47 · see citing works
Rapid double 8‐nm steps by a kinesin mutant
Higuchi, H., Bronner, C. E., Park, H., & Endow, S. A. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600306 · Cited by 50 · see citing works
“Failure to observe the rotational movement predicted by a hand-over-hand mechanism has led to the proposal of an ‘inchworm’ model in which only one head binds to the microtubule and hydrolyzes ATP, dragging the second head along ( Hua et al, 2002 ).”
BackgroundResultInfluentialOn the hand-over-hand mechanism of kinesin
Shao, Q., & Gao, Y. Q. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602828103 · Cited by 48 · see citing works
Coordination of kinesin's two heads studied with mutant heterodimers
Kaseda, K., Higuchi, H., & Hirose, K. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.252409199 · Cited by 47 · see citing works
Kinesin motors as molecular machines.
Endow, S. (2003) · Bioessays · doi:10.1002/bies.10358 · Cited by 47 · see citing works
“However, some researchers have proposed amodel in which only one of the twoheads hydrolyzesATPandadvances in an ‘‘inchworm’’ fashion along the microtubule, dragging the second head along.((47)) This model was proposed because of the failure to detect the alternating rotational movement predicted for a hand-over-hand m…”
BackgroundTama, F., Feig, M., Liu, J., Brooks, C. L., & Taylor, K. A. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.10.084 · Cited by 52 · see citing works
“It is commonly thought that processive movement using a hand-over-hand mechanism involves alternating twisting motions of 1808 about the coiled coil.(74) However, by analogy to the motion modelled here for smooth muscle myosin, this might instead be accomplished by twisting motions about the individual a-helices of th…”
BackgroundSingle Fungal Kinesin Motor Molecules Move Processively along Microtubules
Lakämper, S., Kallipolitou, A., Woehlke, G., Schliwa, M., & Meyhöfer, E. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74991-1 · Cited by 44 · see citing works
Kinesin Walks the Line: Single Motors Observed by Atomic Force Microscopy
Schaap, I. A. T., Carrasco, C., de Pablo, P. J., & Schmidt, C. F. (2011) · Biophysical Journal · doi:10.1016/j.bpj.2011.04.015 · Cited by 42 · see citing works
Protonmotive force: development of electrostatic drivers for synthetic molecular motors.
Crowley, J., Steele, I., & Bosnich, B. (2006) · Chemistry · doi:10.1002/chem.200500519 · Cited by 42 · see citing works
N‐Terminal Kinesins: Many and Various
Wozniak, M. J., Milner, R. D. B., & Allan, V. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.00191.x · Cited by 35 · see citing works
“proposed: the hand-over-hand model (22–24) and the inchworm model (25).”
BackgroundMethodHoward, J. (2007) · Springer eBooks · doi:10.1007/3-540-45701-1_2 · Cited by 27 · see citing works
Gutiérrez-Medina, B., Fehr, A. N., & Block, S. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907133106 · Cited by 37 · see citing works
“Consistent with this model, a landmark experiment by the Gelles group (8) that tracked the angular motions of MTs driven by single kinesin motors affixed to a surface did not find evidence for large-scale rotations.”
BackgroundResultInfluentialJiménez-Zaragoza, M., Yubero, M. L., Martín-Forero, E., Castón, J. R., Reguera, D., Luque, D., de Pablo, P. D., & Rodríguez, J. M. (2018) · eLife · doi:10.7554/elife.37295 · Cited by 35
“, 1997; Perrino and Garcia, 2016) and measurement (Hua et al., 2002; Alsteens et al., 2017) of forces on single molecules are key methodologies to decipher the function of biomolecular systems.”
BackgroundMartin, D. S., Fathi, R., Mitchison, T. J., & Gelles, J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914924107 · Cited by 33 · see citing works
“If interactions with the E-hook prevent this neck rotation as the trailing head steps forward, kinesin would be forced to adopt an asymmetric mechanism in which the three-dimensional structures of the kinesin-microtubule complex differ in even- and odd-numbered steps, and the two heads alternately step past the neck o…”
BackgroundSelf-citationZhang, Y., Chang, Z., Zhao, H., Crespi, S., Feringa, B., & Zhao, D.-P. (2020) · Chem · doi:10.1016/j.chempr.2020.07.025 · Cited by 34
Myosin-V motility: these levers were made for walking.
Tyska, M., & Mooseker, M. (2003) · Trends in Cell Biology · doi:10.1016/s0962-8924(03)00172-7 · Cited by 33 · see citing works
Myosin-V makes two brownian 90° rotations per 36-nm step
Komori, Y., Iwane, A. H., & Yanagida, T. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1298 · Cited by 31 · see citing works
“Kinesin, which also has two heads and moves processively along a microtubule by a hand-over-hand mechanism, does not show rotation during the ste”
BackgroundMaes, C., & van Wieren, M. H. (2003) · Journal of Statistical Physics · doi:10.1023/a:1023691923564 · Cited by 31 · see citing works
The path to visualization of walking myosin V by high-speed atomic force microscopy
Kodera, N., & Ando, T. (2014) · Biophysical Reviews · doi:10.1007/s12551-014-0141-7 · Cited by 35 · see citing works
“This ruled out some models of M5motility such as the ‘inchworm’-like model considered for kinesin (Hua et al. 2002) and the “biased diffusion” model proposed for single-headed myosin II (Kitamura et al. 1999) and single-headedM5 (Okada et al. 2007).”
Bioinspired laser-operated molecular locomotive.
Wang, Z.-S. (2004) · Physical review. E, Statistical, nonlinear, and soft matter physics · doi:10.1103/physreve.70.031903 · Cited by 30
A biologically inspired ratchet model of two coupled Brownian motors
Dan, D., Jayannavar, A., & Menon, G. I. (2002) · doi:10.1016/s0378-4371(02)01400-0 · Cited by 30
Molecular Machines Like Myosin Use Randomness to Behave Predictably
Karagiannis, P., Ishii, Y., & Yanagida, T. (2014) · Chemical Reviews · doi:10.1021/cr400344n · Cited by 31 · see citing works
Zhang, Z., Goldtzvik, Y., & Thirumalai, D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706014114 · Cited by 30 · see citing works
“Unless experiments can track the molecular events in the motor head on shorter time scales (∼ (5-10) μs) one cannot unambiguously assess the interplay of power stroke (involving a structural change in the neck linker) and stochastic motion of the tethered head in resolving the 8 nm step of kinesin.”
Functional asymmetry in kinesin and dynein dimers
Rank, K. C., & Rayment, I. (2012) · Biology of the Cell · doi:10.1111/boc.201200044 · Cited by 23 · see citing works
“The Gelles group demonstrated that microtubules do not rotate in response to stepping by a Kinesin-1 attached to a coverslip through a torsionally stiff coiled coil (Hua et al., 2002).”
BackgroundStudying Individual Events in Biology
Wennmalm, S., & Simon, S. M. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.062305.094225 · Cited by 25 · see citing works
Theoretical model for motility and processivity of two-headed molecular motors
Kanada, R., & Sasaki, K. (2003) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.67.061917 · Cited by 22 · see citing works
Beausang, J., Sun, Y.-J., Quinlan, M., Forkey, J., & Goldman, Y. (2012) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top069344 · Cited by 26
Single molecule processes on the stepwise movement of ATP-driven molecular motors
Nishiyama, M., Higuchi, H., Ishii, Y., Taniguchi, Y., & Yanagida, T. (2003) · Biosystems · doi:10.1016/s0303-2647(03)00122-9 · Cited by 30 · see citing works
Processive Movement by a Kinesin Heterodimer with an Inactivating Mutation in One Head
Thoresen, T., & Gelles, J. (2008) · Biochemistry · doi:10.1021/bi800747e · Cited by 21 · see citing works
“The combined results from a series of studies (10, 12-17) show that kinesin heads move by an alternating-sites handover-hand mechanism, in which the two heads alternately hydrolyze ATP and each head moves forward 16 nm along”
BackgroundSelf-citationCrevenna, A. H., Madathil, S., Cohen, D. N., Wagenbach, M., Fahmy, K., & Howard, J. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.132449 · Cited by 23 · see citing works
“A caveat is that the compliance is attributable to end effects: either the attachment to the cargo surface might be compliant ( 26 ), or the motor domain might transiently detach and rotate before reattaching.”
BackgroundNath, S. (2006) · doi:10.1016/j.procbio.2006.07.003 · Cited by 22
“The mechanism is also consistent with other innovative experiments that showed <308 relative rotation between microtubule and the neck/stalk of kinesin [43].”
ResultMolecular machines directly observed by high‐speed atomic force microscopy
Ando, T. (2013) · FEBS Letters · doi:10.1016/j.febslet.2012.12.024 · Cited by 21
“Thus, the “inchworm” mechanism (a molecule moves forward like an inchworm, in which one head always leads while the other head follows) considered for kinesin [50] as well as the “biased diffusion” mechanism (a molecule moves forward by directional diffusion according to the hypothetical potential slope created along…”
BackgroundSuper-Accuracy and Super-Resolution
Toprak, E., Kural, C., & Selvin, P. R. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(10)75001-1 · Cited by 24 · see citing works
“One of the proposed models, known as the inchworm model, suggested that one of the two heads of kinesin was taking an 8.3 nm step and the other head followed this by another concerted 8.3 nm movement (Hua et al., 2002; Yildiz et al., 2004a).”
MethodInfluentialAssembled capsules transportation driven by motor proteins.
Song, W.-X., He, Q., Cui, Y., Möhwald, H., Diez, S., & Li, J.-B. (2009) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2008.11.136 · Cited by 19 · see citing works
Model for hand-over-hand motion of molecular motors
Munárriz, J., Mazo, J. J., & Falo, F. (2008) · Physical Review E · doi:10.1103/physreve.77.031915 · Cited by 16 · see citing works
Computational modelling of the stochastic dynamics of kinesin biomolecular motors
Jamali, Y., Lohrasebi, A., & Rafii‐Tabar, H. (2007) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2007.03.022 · Cited by 18 · see citing works
Processive behaviour of kinesin observed using micro-fabricated cantilevers
Scholz, T., Vicary, J. A., Jeppesen, G. M., Ulčinas, A., Hörber, J. K. H., & Antognozzi, M. (2011) · Nanotechnology · doi:10.1088/0957-4484/22/9/095707 · Cited by 16 · see citing works
An account of a century of ATP research
Nath, S. (2025) · Biosystems · doi:10.1016/j.biosystems.2025.105527 · Cited by 17 · see citing works
Guo, S., Wang, W.-C., Wang, P., & Xie, P. (2019) · Molecules · doi:10.3390/molecules24020287 · Cited by 18 · see citing works
“of the coiled-coil stalk is kept very stable, without unwinding [46], and moreover the stalk is kept in the fixed orientation [47,48].”
BackgroundProcessive cytoskeletal motors studied with single‐molecule fluorescence techniques
Belyy, V., & Yıldız, A. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.05.040 · Cited by 19 · see citing works
Mechanism for unidirectional movement of kinesin
Xie, P., Dou, S.-X., & Wang, P.-Y. (2003) · Chinese Physics · doi:10.1088/1009-1963/14/4/017 · Cited by 17 · see citing works
Anurag, M., Singh, G., & Dash, D. (2012) · Molecular Biosystems · doi:10.1039/c1mb05210a · Cited by 17 · see citing works
The Orphan Kinesin PAKRP2 Achieves Processive Motility via a Noncanonical Stepping Mechanism
Gicking, A. M., Wang, P., Liu, C., Mickolajczyk, K. J., Guo, L., Hancock, W. O., & Qiu, W. (2019) · Biophysical Journal · doi:10.1016/j.bpj.2019.02.019 · Cited by 21 · see citing works
The mechanical properties of kinesin-1: a holistic approach
Jeppesen, G. M., & Hoerber, J. (2012) · Biochemical Society Transactions · doi:10.1042/bst20110768 · Cited by 14 · see citing works
Intrinsically unidirectional chemically fuelled rotary molecular motors
Mo, K., Zhang, Y., Dong, Z., Yang, Y., Ma, X.-Q., Feringa, B., & Zhao, D.-P. (2022) · Nature · doi:10.1038/s41586-022-05033-0 · Cited by 15 · see citing works
Retracted
- Authors
- Hua, W., Chung, J., & Gelles, J.
- Affiliations
- Biophysics and Structural Biology Program,
- Brandeis University (US)
- Corresponding author
- Gelles, Jeff
- Venue
- Science
- Published
- 2002-02
- Volume
- 295
- Issue
- 5556
- Pages
- 844-848
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1589896765
- Cited by
- 194
- References
- 0
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 4 · 2018: 5 · 2017: 4 · 2016: 7 · 2015: 3 · 2014: 10 · 2013: 4 · 2012: 14
- FWCI
- 7.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Force Microscopy Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Keywords
- kinesin, inchworm mechanism, hand-over-hand mechanism, torsional stiffness, microtubule sliding
- MeSH terms
- Adenosine Triphosphate, Adenylyl Imidodiphosphate, Animals, Binding Sites, Catalysis, Drosophila, Enzymes, Immobilized, Microtubules, Models, Biological, Movement, Rotation, Kinesins, Protein Structure, Tertiary, Dimerization, Streptavidin, Molecular Motor Proteins
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