Motor Coordination via a Tug-of-War Mechanism Drives Bidirectional Vesicle Transport

Current Biology

Volumn 20, Issue 8, 2010, Pages 697-702

  Hendricks, Adam G ^a   Perlson, Eran ^a   Ross, Jennifer L ^b   Schroeder III, Harry W ^a   Tokito, Mariko ^a   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

CELLBIO

Indexed keywords

DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; HYBRID PROTEIN; KINESIN; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL; ARTICLE; CYTOLOGY; GENETICS; MECHANICAL STRESS; METABOLISM; MICROTUBULE; MOUSE; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE; ULTRASTRUCTURE;

ANIMALS; BIOLOGICAL TRANSPORT; DYNEINS; KINESIN; MICE; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURONS; RECOMBINANT FUSION PROTEINS; STRESS, MECHANICAL; TRANSPORT VESICLES;

EID: 77951206786     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2010.02.058     Document Type: Article

References (29)

1. Holzbaur E.L., and Goldman Y.E. Coordination of molecular motors: From in vitro assays to intracellular dynamics. Curr. Opin. Cell Biol. 22 (2010) 4-13
2. Ross J.L., Wallace K., Shuman H., Goldman Y.E., and Holzbaur E.L. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 8 (2006) 562-570
3. Caviston J.P., Ross J.L., Antony S.M., Tokito M., and Holzbaur E.L. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. USA 104 (2007) 10045-10050
4. Miller R.H., and Lasek R.J. Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm. J. Cell Biol. 101 (1985) 2181-2193
5. Cui B., Wu C., Chen L., Ramirez A., Bearer E.L., Li W.P., Mobley W.C., and Chu S. One at a time, live tracking of NGF axonal transport using quantum dots. Proc. Natl. Acad. Sci. USA 104 (2007) 13666-13671
6. Kardon J.R., Reck-Peterson S.L., and Vale R.D. Regulation of the processivity and intracellular localization of Saccharomyces cerevisiae dynein by dynactin. Proc. Natl. Acad. Sci. USA 106 (2009) 5669-5674
7. Ashkin A., Schütze K., Dziedzic J.M., Euteneuer U., and Schliwa M. Force generation of organelle transport measured in vivo by an infrared laser trap. Nature 348 (1990) 346-348
8. Gross S.P. Hither and yon: A review of bi-directional microtubule-based transport. Phys. Biol. 1 (2004) R1-R11
9. Shubeita G.T., Tran S.L., Xu J., Vershinin M., Cermelli S., Cotton S.L., Welte M.A., and Gross S.P. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell 135 (2008) 1098-1107
10. Sims P.A., and Xie X.S. Probing dynein and kinesin stepping with mechanical manipulation in a living cell. ChemPhysChem 10 (2009) 1511-1516
11. Soppina V., Rai A.K., Ramaiya A.J., Barak P., and Mallik R. Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc. Natl. Acad. Sci. USA 106 (2009) 19381-19386
12. Nelson S.R., Ali M.Y., Trybus K.M., and Warshaw D.M. Random walk of processive, quantum dot-labeled myosin Va molecules within the actin cortex of COS-7 cells. Biophys. J. 97 (2009) 509-518
13. Ross J.L., Ali M.Y., and Warshaw D.M. Cargo transport: Molecular motors navigate a complex cytoskeleton. Curr. Opin. Cell Biol. 20 (2008) 41-47
14. Kim H., Ling S.C., Rogers G.C., Kural C., Selvin P.R., Rogers S.L., and Gelfand V.I. Microtubule binding by dynactin is required for microtubule organization but not cargo transport. J. Cell Biol. 176 (2007) 641-651
15. Dixit R., Levy J.R., Tokito M., Ligon L.A., and Holzbaur E.L. Regulation of dynactin through the differential expression of p150Glued isoforms. J. Biol. Chem. 283 (2008) 33611-33619
16. Vaughan P.S., Miura P., Henderson M., Byrne B., and Vaughan K.T. A role for regulated binding of p150(Glued) to microtubule plus ends in organelle transport. J. Cell Biol. 158 (2002) 305-319
17. Ingold A.L., Cohn S.A., and Scholey J.M. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J. Cell Biol. 107 (1988) 2657-2667
18. Loubéry S., Wilhelm C., Hurbain I., Neveu S., Louvard D., and Coudrier E. Different microtubule motors move early and late endocytic compartments. Traffic 9 (2008) 492-509
19. Brown C.L., Maier K.C., Stauber T., Ginkel L.M., Wordeman L., Vernos I., and Schroer T.A. Kinesin-2 is a motor for late endosomes and lysosomes. Traffic 6 (2005) 1114-1124
20. Bananis E., Nath S., Gordon K., Satir P., Stockert R.J., Murray J.W., and Wolkoff A.W. Microtubule-dependent movement of late endocytic vesicles in vitro: Requirements for dynein and kinesin. Mol. Biol. Cell 15 (2004) 3688-3697
21. Müller M.J., Klumpp S., and Lipowsky R. Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc. Natl. Acad. Sci. USA 105 (2008) 4609-4614
22. Stock M.F., Guerrero J., Cobb B., Eggers C.T., Huang T.G., Li X., and Hackney D.D. Formation of the compact confomer of kinesin requires a COOH-terminal heavy chain domain and inhibits microtubule-stimulated ATPase activity. J. Biol. Chem. 274 (1999) 14617-14623
23. Imanishi M., Endres N.F., Gennerich A., and Vale R.D. Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. J. Cell Biol. 174 (2006) 931-937
24. Blasius T.L., Cai D., Jih G.T., Toret C.P., and Verhey K.J. Two binding partners cooperate to activate the molecular motor kinesin-1. J. Cell Biol. 176 (2007) 11-17
25. Hackney D.D., Baek N., and Snyder A.C. Half-site inhibition of dimeric kinesin head domains by monomeric tail domains. Biochemistry 48 (2009) 3448-3456
26. Dixit R., Ross J.L., Goldman Y.E., and Holzbaur E.L. Differential regulation of dynein and kinesin motor proteins by tau. Science 319 (2008) 1086-1089
27. Mallik R., Carter B.C., Lex S.A., King S.J., and Gross S.P. Cytoplasmic dynein functions as a gear in response to load. Nature 427 (2004) 649-652
28. Gillespie D.T. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys. 22 (1976) 403-434
29. Muthukrishnan G., Zhang Y., Shastry S., and Hancock W.O. The processivity of kinesin-2 motors suggests diminished front-head gating. Curr. Biol. 19 (2009) 442-447