© The Rockefeller University Press,
0021-9525/1999//1045 $5.00
The Journal of Cell Biology, Volume 146, Number 5,
, 1999 1045-1060
Myosin VA Movements in Normal and Dilute-Lethal Axons Provide Support for a Dual Filament Motor Complex
P.C. Bridgmana
a Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110
Department of Anatomy and Neurobiology, Box 8108, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110.(314) 747-1150(314) 362-3449
bridgmap{at}thalamus.wustl.edu
To investigate the role that myosin Va plays in axonal transport of organelles, myosin Va–associated organelle movements were monitored in living neurons using microinjected fluorescently labeled antibodies to myosin Va or expression of a green fluorescent protein–myosin Va tail construct. Myosin Va–associated organelles made rapid bi-directional movements in both normal and dilute-lethal (myosin Va null) neurites. In normal neurons, depolymerization of microtubules by nocodazole slowed, but did not stop movement. In contrast, depolymerization of microtubules in dilute-lethal neurons stopped movement. Myosin Va or synaptic vesicle protein 2 (SV2), which partially colocalizes with myosin Va on organelles, did not accumulate in dilute-lethal neuronal cell bodies because of an anterograde bias associated with organelle transport. However, SV2 showed peripheral accumulations in axon regions of dilute-lethal neurons rich in tyrosinated tubulin. This suggests that myosin Va–associated organelles become stranded in regions rich in dynamic microtubule endings. Consistent with these observations, presynaptic terminals of cerebellar granule cells in dilute-lethal mice showed increased cross-sectional area, and had greater numbers of both synaptic and larger SV2 positive vesicles. Together, these results indicate that myosin Va binds to organelles that are transported in axons along microtubules. This is consistent with both actin- and microtubule-based motors being present on these organelles. Although myosin V activity is not necessary for long-range transport in axons, myosin Va activity is necessary for local movement or processing of organelles in regions, such as presynaptic terminals that lack microtubules.
Key Words: myosin Va actin microtubules organelles dilute-lethal
© 1999 The Rockefeller University Press
1.used in this paper: BDS, biological detection systems; Cy3, indocarbocyanine; GFP, green fluorescent protein; iu, intensity units; SCG, superior cervical ganglion; SV2, synaptic vesicle protein 2

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Wozniak, M. J., Bola, B., Brownhill, K., Yang, Y.-C., Levakova, V., Allan, V. J.
(2009). Role of kinesin-1 and cytoplasmic dynein in endoplasmic reticulum movement in VERO cells. J. Cell Sci.
122: 1979-1989
[Abstract]
[Full Text]
-
Alami, N. H., Jung, P., Brown, A.
(2009). Myosin Va Increases the Efficiency of Neurofilament Transport by Decreasing the Duration of Long-Term Pauses. J. Neurosci.
29: 6625-6634
[Abstract]
[Full Text]
-
Qian Cai, , Sheng, Z.-H.
(2009). Molecular Motors and Synaptic Assembly. Neuroscientist
15: 78-89
[Abstract]
-
Balastik, M., Ferraguti, F., Pires-da Silva, A., Lee, T. H., Alvarez-Bolado, G., Lu, K. P., Gruss, P.
(2008). Deficiency in ubiquitin ligase TRIM2 causes accumulation of neurofilament light chain and neurodegeneration. Proc. Natl. Acad. Sci. USA
105: 12016-12021
[Abstract]
[Full Text]
-
Watanabe, S., Watanabe, T. M., Sato, O., Awata, J., Homma, K., Umeki, N., Higuchi, H., Ikebe, R., Ikebe, M.
(2008). Human Myosin Vc Is a Low Duty Ratio Nonprocessive Motor. J. Biol. Chem.
283: 10581-10592
[Abstract]
[Full Text]
-
Slepchenko, B. M., Semenova, I., Zaliapin, I., Rodionov, V.
(2007). Switching of membrane organelles between cytoskeletal transport systems is determined by regulation of the microtubule-based transport. JCB
179: 635-641
[Abstract]
[Full Text]
-
Sloane, J. A., Vartanian, T. K.
(2007). Myosin Va Controls Oligodendrocyte Morphogenesis and Myelination. J. Neurosci.
27: 11366-11375
[Abstract]
[Full Text]
-
Blard, O., Feuillette, S., Bou, J., Chaumette, B., Frebourg, T., Campion, D., Lecourtois, M.
(2007). Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum Mol Genet
16: 555-566
[Abstract]
[Full Text]
-
Lise, M.-F., Wong, T. P., Trinh, A., Hines, R. M., Liu, L., Kang, R., Hines, D. J., Lu, J., Goldenring, J. R., Wang, Y. T., El-Husseini, A.
(2006). Involvement of Myosin Vb in Glutamate Receptor Trafficking. J. Biol. Chem.
281: 3669-3678
[Abstract]
[Full Text]
-
Hollenbeck, P. J., Saxton, W. M.
(2005). The axonal transport of mitochondria. J. Cell Sci.
118: 5411-5419
[Abstract]
[Full Text]
-
Takagishi, Y., Futaki, S., Itoh, K., Espreafico, E. M., Murakami, N., Murata, Y., Mochida, S.
(2005). Localization of myosin II and V isoforms in cultured rat sympathetic neurones and their potential involvement in presynaptic function. J. Physiol.
569: 195-208
[Abstract]
[Full Text]
-
Watanabe, M., Nomura, K., Ohyama, A., Ishikawa, R., Komiya, Y., Hosaka, K., Yamauchi, E., Taniguchi, H., Sasakawa, N., Kumakura, K., Ushiki, T., Sato, O., Ikebe, M., Igarashi, M.
(2005). Myosin-Va Regulates Exocytosis through the Submicromolar Ca2+-dependent Binding of Syntaxin-1A. Mol. Biol. Cell
16: 4519-4530
[Abstract]
[Full Text]
-
Krendel, M., Mooseker, M. S.
(2005). Myosins: Tails (and Heads) of Functional Diversity. Physiology
20: 239-251
[Abstract]
[Full Text]
-
Varadi, A., Tsuboi, T., Rutter, G. A.
(2005). Myosin Va Transports Dense Core Secretory Vesicles in Pancreatic MIN6 {beta}-Cells. Mol. Biol. Cell
16: 2670-2680
[Abstract]
[Full Text]
-
Yan, Q., Sun, W., Kujala, P., Lotfi, Y., Vida, T. A., Bean, A. J.
(2005). CART: An Hrs/Actinin-4/BERP/Myosin V Protein Complex Required for Efficient Receptor Recycling. Mol. Biol. Cell
16: 2470-2482
[Abstract]
[Full Text]
-
Jung, C., Chylinski, T. M., Pimenta, A., Ortiz, D., Shea, T. B.
(2004). Neurofilament Transport Is Dependent on Actin and Myosin. J. Neurosci.
24: 9486-9496
[Abstract]
[Full Text]
-
Libby, R. T., Lillo, C., Kitamoto, J., Williams, D. S., Steel, K. P.
(2004). Myosin Va is required for normal photoreceptor synaptic activity. J. Cell Sci.
117: 4509-4515
[Abstract]
[Full Text]
-
Du, Y., Ferro-Novick, S., Novick, P.
(2004). Dynamics and inheritance of the endoplasmic reticulum. J. Cell Sci.
117: 2871-2878
[Abstract]
[Full Text]
-
Provance, D. W. Jr., Gourley, C. R., Silan, C. M., Cameron, L. C., Shokat, K. M., Goldenring, J. R., Shah, K., Gillespie, P. G., Mercer, J. A.
(2004). From the Cover: Chemical-genetic inhibition of a sensitized mutant myosin Vb demonstrates a role in peripheral-pericentriolar membrane traffic. Proc. Natl. Acad. Sci. USA
101: 1868-1873
[Abstract]
[Full Text]
-
Cao, T. T., Chang, W., Masters, S. E., Mooseker, M. S.
(2004). Myosin-Va Binds to and Mechanochemically Couples Microtubules to Actin Filaments. Mol. Biol. Cell
15: 151-161
[Abstract]
[Full Text]
-
Lalli, G., Gschmeissner, S., Schiavo, G.
(2003). Myosin Va and microtubule-based motors are required for fast axonal retrograde transport of tetanus toxin in motor neurons. J. Cell Sci.
116: 4639-4650
[Abstract]
[Full Text]
-
Mundy, D. I., Machleidt, T., Ying, Y.-s., Anderson, R. G. W., Bloom, G. S.
(2002). Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci.
115: 4327-4339
[Abstract]
[Full Text]
-
Rao, M. V., Engle, L. J., Mohan, P. S., Yuan, A., Qiu, D., Cataldo, A., Hassinger, L., Jacobsen, S., Lee, V. M-Y., Andreadis, A., Julien, J.-P., Bridgman, P. C., Nixon, R. A.
(2002). Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. JCB
159: 279-290
[Abstract]
[Full Text]
-
Gross, S. P., Tuma, M. C., Deacon, S. W., Serpinskaya, A. S., Reilein, A. R., Gelfand, V. I.
(2002). Interactions and regulation of molecular motors in Xenopus melanophores. JCB
156: 855-865
[Abstract]
[Full Text]
-
Carter, A. R., Chen, C., Schwartz, P. M., Segal, R. A.
(2002). Brain-Derived Neurotrophic Factor Modulates Cerebellar Plasticity and Synaptic Ultrastructure. J. Neurosci.
22: 1316-1327
[Abstract]
[Full Text]
-
Bizario, J. C. S., Castro, F. A., Sousa, J. F., Fernandes, R. N., Damiao, A. D., Oliveira, M. K., Palma, P. V. B., Larson, R. E., Voltarelli, J. C., Espreafico, E. M.
(2002). Myosin-V colocalizes with MHC class II in blood mononuclear cells and is up-regulated by T-lymphocyte activation. J. Leukoc. Biol.
71: 195-204
[Abstract]
[Full Text]
-
Cordonnier, M.-N., Dauzonne, D., Louvard, D., Coudrier, E.
(2001). Actin Filaments and Myosin I Alpha Cooperate with Microtubules for the Movement of Lysosomes. Mol. Biol. Cell
12: 4013-4029
[Abstract]
[Full Text]
-
Tauhata, S. B. F., dos Santos, D. V., Taylor, E. W., Mooseker, M. S., Larson, R. E.
(2001). High Affinity Binding of Brain Myosin-Va to F-actin Induced by Calcium in the Presence of ATP. J. Biol. Chem.
276: 39812-39818
[Abstract]
[Full Text]
-
Al-Haddad, A., Shonn, M. A., Redlich, B., Blocker, A., Burkhardt, J. K., Yu, H., Hammer, J. A. III, Weiss, D. G., Steffen, W., Griffiths, G., Kuznetsov, S. A.
(2001). Myosin Va Bound to Phagosomes Binds to F-Actin and Delays Microtubule-dependent Motility. Mol. Biol. Cell
12: 2742-2755
[Abstract]
[Full Text]
-
Lapierre, L. A., Kumar, R., Hales, C. M., Navarre, J., Bhartur, S. G., Burnette, J. O., Provance, D. W. Jr., Mercer, J. A., Bahler, M., Goldenring, J. R.
(2001). Myosin Vb Is Associated with Plasma Membrane Recycling Systems. Mol. Biol. Cell
12: 1843-1857
[Abstract]
[Full Text]
-
Motegi, F., Arai, R., Mabuchi, I.
(2001). Identification of Two Type V Myosins in Fission Yeast, One of Which Functions in Polarized Cell Growth and Moves Rapidly in the Cell. Mol. Biol. Cell
12: 1367-1380
[Abstract]
[Full Text]
-
Schnell, E., Nicoll, R. A.
(2001). Hippocampal Synaptic Transmission and Plasticity Are Preserved in Myosin Va Mutant Mice. J. Neurophysiol.
85: 1498-1501
[Abstract]
[Full Text]
-
Sato, Y, Wada, M, Kadota, A
(2001). Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. J. Cell Sci.
114: 269-279
[Abstract]
-
Olkkonen, V. M., Ikonen, E.
(2000). Genetic Defects of Intracellular-Membrane Transport. NEJM
343: 1095-1104
[Full Text]
-
Catlett, N. L., Duex, J. E., Tang, F., Weisman, L. S.
(2000). Two Distinct Regions in a Yeast Myosin-V Tail Domain Are Required for the Movement of Different Cargoes. JCB
150: 513-526
[Abstract]
[Full Text]
-
Naisbitt, S., Valtschanoff, J., Allison, D. W., Sala, C., Kim, E., Craig, A. M., Weinberg, R. J., Sheng, M.
(2000). Interaction of the Postsynaptic Density-95/Guanylate Kinase Domain-Associated Protein Complex with a Light Chain of Myosin-V and Dynein. J. Neurosci.
20: 4524-4534
[Abstract]
[Full Text]
-
Kaether, C., Skehel, P., Dotti, C. G.
(2000). Axonal Membrane Proteins Are Transported in Distinct Carriers: A Two-Color Video Microscopy Study in Cultured Hippocampal Neurons. Mol. Biol. Cell
11: 1213-1224
[Abstract]
[Full Text]
-
Stachelek, S. J., Kowalik, T. F., Farwell, A. P., Leonard, J. L.
(2000). Myosin V Plays an Essential Role in the Thyroid Hormone-dependent Endocytosis of Type II Iodothyronine 5'-Deiodinase. J. Biol. Chem.
275: 31701-31707
[Abstract]
[Full Text]
-
Stachelek, S. J., Tuft, R. A., Lifschitz, L. M., Leonard, D. M., Farwell, A. P., Leonard, J. L.
(2001). Real-time Visualization of Processive Myosin 5a-mediated Vesicle Movement in Living Astrocytes. J. Biol. Chem.
276: 35652-35659
[Abstract]
[Full Text]
-
Gross, S. P., Tuma, M. C., Deacon, S. W., Serpinskaya, A. S., Reilein, A. R., Gelfand, V. I.
(2002). Interactions and regulation of molecular motors in Xenopus melanophores. JCB
156: 855-865
[Abstract]
[Full Text]