On the Hand-over-hand Mechanism of Kinesin

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2006 May 16

PMID 16698919

Citations 11

Authors

Qiang Shao

Yi Qin Gao

Affiliations

Soon will be listed here.

Abstract

We present here a simple theoretical model for conventional kinesin. The model reproduces the hand-over-hand mechanism for kinesin walking to the plus end of a microtubule. A large hindering force induces kinesin to walk slowly to the minus end, again by a hand-over-hand mechanism. Good agreement is obtained between the calculated and experimental results on the external force dependence of the walking speed, the forward/backward step ratio, and dwell times for both forward and backward steps. The model predicts that both forward and backward motions of kinesin take place at the same chemical state of the motor heads, with the front head being occupied by an ATP (or ADP,Pi) and the rear being occupied by an ADP. The direction of motion is a result of the competition between the power stroke produced by the front head and the external load. The other predictions include the external force dependence of the chemomechanical coupling ratio (e.g., the stepping distance/ATP ratio) and the walking speed of kinesin at force ranges that have not been tested by experiments. The model predicts that the chemomechanical coupling remains tight in a large force range. However, when the external force is very large (e.g., approximately 18 pN), kinesin slides in an inchworm fashion, and the translocation of kinesin becomes loosely coupled to ATP turnovers.

Citing Articles

Organization of two kinesins in a two-dimensional microtubule network.

Bergues J, Falo F PLoS One. 2024; 19(3):e0295652.

PMID: 38478520 PMC: 10936800. DOI: 10.1371/journal.pone.0295652.

Magic-angle-spinning NMR structure of the kinesin-1 motor domain assembled with microtubules reveals the elusive neck linker orientation.

Zhang C, Guo C, Russell R, Quinn C, Li M, Williams J Nat Commun. 2022; 13(1):6795.

PMID: 36357375 PMC: 9649657. DOI: 10.1038/s41467-022-34026-w.

Mechanistic basis of propofol-induced disruption of kinesin processivity.

Dutta M, Gilbert S, Onuchic J, Jana B Proc Natl Acad Sci U S A. 2021; 118(5).

PMID: 33495322 PMC: 7865149. DOI: 10.1073/pnas.2023659118.

Structural consequences of hereditary spastic paraplegia disease-related mutations in kinesin.

Dutta M, Diehl M, Onuchic J, Jana B Proc Natl Acad Sci U S A. 2018; 115(46):E10822-E10829.

PMID: 30366951 PMC: 6243270. DOI: 10.1073/pnas.1810622115.

Processivity of dimeric kinesin-1 molecular motors.

Guo S, Shi X, Wang P, Xie P FEBS Open Bio. 2018; 8(8):1332-1351.

PMID: 30087836 PMC: 6070657. DOI: 10.1002/2211-5463.12486.

References

Asbury C, Fehr A, Block S . Kinesin moves by an asymmetric hand-over-hand mechanism. Science. 2003; 302(5653):2130-4. PMC: 1523256. DOI: 10.1126/science.1092985. View

Hua W, Chung J, Gelles J . Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements. Science. 2002; 295(5556):844-8. DOI: 10.1126/science.1063089. View

Schnitzer M, Block S . Kinesin hydrolyses one ATP per 8-nm step. Nature. 1997; 388(6640):386-90. DOI: 10.1038/41111. View

Yun M, Bronner C, Park C, Cha S, Park H, Endow S . Rotation of the stalk/neck and one head in a new crystal structure of the kinesin motor protein, Ncd. EMBO J. 2003; 22(20):5382-9. PMC: 213785. DOI: 10.1093/emboj/cdg531. View

Hackney D . Kinesin ATPase: rate-limiting ADP release. Proc Natl Acad Sci U S A. 1988; 85(17):6314-8. PMC: 281960. DOI: 10.1073/pnas.85.17.6314. View

Astumian R . The role of thermal activation in motion and force generation by molecular motors. Philos Trans R Soc Lond B Biol Sci. 2000; 355(1396):511-22. PMC: 1692764. DOI: 10.1098/rstb.2000.0592. View

Nishiyama M, Higuchi H, Yanagida T . Chemomechanical coupling of the forward and backward steps of single kinesin molecules. Nat Cell Biol. 2002; 4(10):790-7. DOI: 10.1038/ncb857. View

Mallik R, Carter B, Lex S, King S, Gross S . Cytoplasmic dynein functions as a gear in response to load. Nature. 2004; 427(6975):649-52. DOI: 10.1038/nature02293. View

Carter N, Cross R . Mechanics of the kinesin step. Nature. 2005; 435(7040):308-12. DOI: 10.1038/nature03528. View

10.

Schnitzer M, Visscher K, Block S . Force production by single kinesin motors. Nat Cell Biol. 2000; 2(10):718-23. DOI: 10.1038/35036345. View

11.

Peskin C, Oster G . Coordinated hydrolysis explains the mechanical behavior of kinesin. Biophys J. 1995; 68(4 Suppl):202S-210S; discussion 210S-211S. PMC: 1281917. View

12.

Coppin C, Finer J, Spudich J, Vale R . Detection of sub-8-nm movements of kinesin by high-resolution optical-trap microscopy. Proc Natl Acad Sci U S A. 1996; 93(5):1913-7. PMC: 39882. DOI: 10.1073/pnas.93.5.1913. View

13.

Cross R, Crevel I, Carter N, Alonso M, Hirose K, Amos L . The conformational cycle of kinesin. Philos Trans R Soc Lond B Biol Sci. 2000; 355(1396):459-64. PMC: 1692756. DOI: 10.1098/rstb.2000.0587. View

14.

Kawaguchi K, Ishiwata S . Nucleotide-dependent single- to double-headed binding of kinesin. Science. 2001; 291(5504):667-9. DOI: 10.1126/science.291.5504.667. View

15.

Hirokawa N . Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 1998; 279(5350):519-26. DOI: 10.1126/science.279.5350.519. View

16.

Kolomeisky A, Stukalin E, Popov A . Understanding mechanochemical coupling in kinesins using first-passage-time processes. Phys Rev E Stat Nonlin Soft Matter Phys. 2005; 71(3 Pt 1):031902. DOI: 10.1103/PhysRevE.71.031902. View

17.

Thomas N, Imafuku Y, Kamiya T, Tawada K . Kinesin: a molecular motor with a spring in its step. Proc Biol Sci. 2002; 269(1507):2363-71. PMC: 1691169. DOI: 10.1098/rspb.2002.2117. View

18.

Nishiyama M, Muto E, Inoue Y, Yanagida T, Higuchi H . Substeps within the 8-nm step of the ATPase cycle of single kinesin molecules. Nat Cell Biol. 2001; 3(4):425-8. DOI: 10.1038/35070116. View

19.

Coy D, Wagenbach M, Howard J . Kinesin takes one 8-nm step for each ATP that it hydrolyzes. J Biol Chem. 1999; 274(6):3667-71. DOI: 10.1074/jbc.274.6.3667. View

20.

Ma Y, Taylor E . Kinetic mechanism of a monomeric kinesin construct. J Biol Chem. 1997; 272(2):717-23. DOI: 10.1074/jbc.272.2.717. View