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Microtubule Motors in Cell and Tissue Function

Michael P. Sheetz

10.1002/cphy.cp140113

Source: Supplement 31: Handbook of Physiology, Cell Physiology

Originally published: 1997

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Why Motors—and Where—in Tissues?
2 Basic Cellular Motor Mechanisms
3 Organization of Microtubules in Tissues
4 Organelle‐Motor Complexes
5 Microtubule Motor Structure
6 Mechanism of Conversion of ATP Energy into Motility
7 Summary
Figure 1. Figure 1.

This illustrates three types of microtubule organization. The single microtubule organizing center (centrosome) in fibroblasts produces a radial array of microtubules with their plus ends toward the periphery. In epithelial cells, multiple microtubule organizing centers in the apical region give rise to a parallel array of microtubules. Within axons there is a third pattern of overlapping microtubules with all of their plus ends toward the periphery, thus forming a continuous path from the cell body to the synapse.
Figure 2. Figure 2.

This diagram illustrates the basic structure of the motors and the known components of the organelle motor complex. Kinectin is a membrane‐attached protein and appears to bind or interact with both motors. Dynactin activates organelle motility for only cytoplasmic dynein and has centractin bound to it which could interact with other myosin motility systems. There are probably many additional components that contribute to the regulation of organelle motility, these include the MAPs on the microtubule, which could block motor interactions with the microtubule.


Figure 1.

This illustrates three types of microtubule organization. The single microtubule organizing center (centrosome) in fibroblasts produces a radial array of microtubules with their plus ends toward the periphery. In epithelial cells, multiple microtubule organizing centers in the apical region give rise to a parallel array of microtubules. Within axons there is a third pattern of overlapping microtubules with all of their plus ends toward the periphery, thus forming a continuous path from the cell body to the synapse.



Figure 2.

This diagram illustrates the basic structure of the motors and the known components of the organelle motor complex. Kinectin is a membrane‐attached protein and appears to bind or interact with both motors. Dynactin activates organelle motility for only cytoplasmic dynein and has centractin bound to it which could interact with other myosin motility systems. There are probably many additional components that contribute to the regulation of organelle motility, these include the MAPs on the microtubule, which could block motor interactions with the microtubule.

References
 1. Allen, R. D., N. S. Allen, and J. L. Travis. Video‐enhanced contrast, differential interference contrast (AVEC‐DIC) microscopy: a new method capable of analyzing microtubule related motility in the reticulopodial network of Allogromia laticollans. Cell Motil. 1: 291–302, 1981.
 2. Allen, R. D., D. G. Weiss, J. H. Hayden, D. T. Brown, H. Fujiwake, M. Simpson. Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport. J. Cell Biol. 100: 1736–1752, 1985.
 3. Allen, R. D., J. Metuzals, I. Tasaki, S. T. Brady, and S. P. Gilbert. Fast axonal transport in squid giant axon. Science 218: 1127–1129, 1982.
 4. Baas, P. W., J. S. Deitch, M. M. Black, and G. A. Banker. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. U.S.A. 85: 8335–8339, 1988.
 5. Brady, S. T. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317: 73–75, 1985.
 6. Dabora, S. L., and M. P. Sheetz. The microtubule‐dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts. Cell 54: 27–35, 1988.
 7. Endow, S. A., and M. A. Titus. Genetic approaches to molecular motors [Review]. Annu. Rev. Cell Biol. 8: 29–66, 1992.
 8. Fuller, M. T., and P. G. Wilson. Force and counterforce in the mitotic spindle [Review]. Cell 71: 547–50, 1992.
 9. Gibbons, I. R. Dynein ATPases as microtubule motors [Review]. J. Biol. Chem. 263: 15837–15840, 1988.
 10. Goldstein, L. S. With apologies to Scheherazade: tails of 1001 kinesin motors [Review]. Annu. Rev. Genet. 27: 319–351, 1993.
 11. Hirokawa, N. Mechanism of axonal transport. Identification of new molecular motors and regulations of transports [Review]. Neurosci. Res. 18: 1–9, 1993.
 12. Holzbaur, E. L., J. A. Hammarback, B. M. Paschal, N. G. Kravit, K. K. Pfister, and R. B. Vallee. Homology of a 150K cytoplasmic dynein‐associated polypeptide with the Drosophila gene Glued [published erratum appears in Nature 1992 Dec 17;360(6405):695]. Nature 351: 579–583, 1991.
 13. Hoyt, M. A. Cellular roles of kinesin and related proteins [Review]. Curr. Opin. Cell Biol. 6: 63–68, 1994.
 14. Inoue, S. Video image processing greatly enhances contrast, quality, and speed in polarization‐based microscopy. j. Cell Biol. 89: 346–356, 1981.
 15. Jellali, A., B. M. Metz, I. Surgucheva, V. Jancsik, C. Schwartz, D. Filliol, V. I. Gelfand, and A. Rendon. Structural and biochemical properties of kinesin heavy chain associated with rat brain mitochondria. Cell Motil. Cytoskeleton 28: 79–93, 1994.
 16. Kondo, S., Y. R. Sato, Y. Noda, H. Aizawa, T. Nakata, Y. Matsuura, and N. Hirokawa. KIF3A is a new microtubule‐based anterograde motor in the nerve axon. J. Cell Biol. 125: 1095–1107, 1994.
 17. Kuo, S. C., and M. P. Sheetz. Force of single kinesin molecules measured with optical tweezers. Science 260: 232–234, 1993.
 18. Lasek, R. J., and S. T. Brady. Adenylyl imidodiphosphate (AMP‐PNP), a non‐hydrolyzable analogue of ATP produces a stable intermediate in the motility cycle of fast axonal transport. Nature 316: 645–647, 1985.
 19. Lillie, S. H., and S. S. Brown. Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin‐related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae. J. Cell Biol. 125: 825–842, 1994.
 20. Lopez, L. A., and M. P. Sheetz. Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil. Cytoskeleton 24: 1–16, 1993.
 21. Luby‐Phelps, K., and D. L. Taylor. Subcellular compartmentalization by local differentiation of cytoplasmic structure. Cell Motil. Cytoskeleton 10: 28–37, 1988.
 22. Lye, R. J., M. E. Porter, J. M. Scholey, and J. R. Mclntosh. Identification of a microtubule‐based cytoplasmic motor in the nematode C. elegans. Cell 51: 309–318, 1987.
 23. Mclntosh, J. R., and C. M. Pfarr. Mitotic motors [Review]. J. Cell Biol. 115: 577–585, 1991.
 24. Paschal, B. M., H. S. Shpetner, and R. B. Vallee. MAP 1C is a microtubule‐activated ATPase which translocates microtubules in vitro and has dynein‐like properties. J. Cell Biol. 105: 1273–1282, 1987.
 25. Patel, N., M. D. Thierry, and J. R. Mancillas. Cloning by insertional mutagenesis of a cDNA encoding Caenorhabditis elegans kinesin heavy chain. Proc. Natl. Acad. Sci. U.S.A. 90: 9181–9185, 1993.
 26. Schnapp, B. J., T. S. Reese, and R. Bechtold. Kinesin is bound with high affinity to squid axon organelles that move to the plus‐end of microtubules. J. Cell Biol. 119: 389–399, 1992.
 27. Schnapp, B. J., R. D. Vale, M. P. Sheetz, and T. S. Reese. Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell 40: 455–462, 1985.
 28. Scholey, J. M., M. E. Porter, P. M. Grissom, and J. R. Mclntosh. Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature 318: 483–486, 1985.
 29. Schroer, T. A. New insights into the interaction of cytoplasmic dynein with the actin‐related protein, Arp 1 [Review]. J. Cell Biol. 127: 1–4, 1994.
 30. Schroer, T. A. Structure, function and regulation of cytoplasmic dynein. [Review]. Curr. Opin, Cell Biol. 6: 69–73, 1994.
 31. Schroer, T. A., and M. P. Sheetz. Functions of microtubule‐based motors. Annu. Rev. Physiol. 53: 629–652, 1991.
 32. Schroer, T. A., and M. P. Sheetz. Two activators of microtubule‐based vesicle transport. J. Cell Biol. 115: 1309–1318.
 33. Sekine, Y., Y. Okada, Y. Noda, S. Kondo, H. Aizawa, R. Takemura, and N. Hirokawa. A novel microtubule‐based motor protein (KIF4) for organelle transports, whose expression is regulated developmentally. J. Cell Biol. 127: 187–201, 1994.
 34. Shakir, M. A., T. Fukushige, H. Yasuda, J. Miwa, and S. S. Siddiqui. C. elegans osm‐3 gene mediating osmotic avoidance behaviour encodes a kinesin‐like protein. Neuroreport 4: 891–894, 1993.
 35. Sheetz, M. P., and J. A. Spudich. Movement of myosin‐coated fluorescent beads on actin cables in vitro. Nature, 303: 31–35, 1983.
 36. Skoufias, D. A., and J. M. Scholey. Cytoplasmic microtubule‐based motor proteins [Review]. Curr. Opin. Cell Biol. 5: 95–104, 1993.
 37. Svoboda, K., and S. M. Block. Force and velocity measured for single kinesin molecules. Cell 77: 773–84, 1994.
 38. Svoboda, K., C. F. Schmidt, B. J. Schnapp, and S. M. Block. Direct observation of kinesin stepping by optical trapping interferometry [see comments]. Nature 365: 721–727, 1993.
 39. Toyoshima, I., H. Yu, E. R. Steuer, and M. P. Sheetz. Kinectin, a major kinesin‐binding protein on ER. J. Cell Biol. 118: 1121–1131, 1992.
 40. Vale, R. D., T. S. Reese, and M. P. Sheetz. Identification of a novel force‐generating protein, kinesin, involved in microtubule‐based motility. Cell 42: 39–50, 1985.
 41. Vale, R. D., B. J. Schnapp, T. S. Reese, and M. P. Sheetz. Organelle, bead, and microtubule translocations promoted by soluble factors from the squid giant axon. Cell 40: 559–569, 1985.
 42. Vale, R. D., B. J. Schnapp, T. Mitchison, E. Steuier, T. S. Reese, M. P. Sheetz. Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell 43: 623–632, 1985.
 43. Vallee, R. Molecular analysis of the microtubule motor dynein [Review]. Proc. Natl. Acad. Sci. U.S.A. 90: 8769–8772, 1993.
 44. Wadsworth, P. Mitosis: spindle assembly and chromosome motion [Review]. Curr. Opin. Cell Biol. 5: 123–128, 1993.
 45. Walker, R. A., and M. P. Sheetz. Cytoplasmic microtubule‐associated motors [Review]. Annu. Rev. Biochem. 62: 429–451, 1993.
 46. Yu, H., C. V. Nicchitta, J. Kumar, M. Becker, I. Toyoshima, and M. P. Sheetz. Characterization of kinectin, a kinesin‐binding protein: primary sequence and N‐terminal topogenic signal analysis. J. Cell Biol. 6: 171–183, 1995.

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Article Title: Microtubule Motors in Cell and Tissue Function
 

How to Cite

Michael P. Sheetz. Microtubule Motors in Cell and Tissue Function. Compr Physiol 2011, Supplement 31: Handbook of Physiology, Cell Physiology: 557-562. First published in print 1997. doi: 10.1002/cphy.cp140113